The Morphology, Ecology, and Conservation Statusof the Local Endemic Species Salsola grandis

Abstract Turkey has a great biodiversity which is threaten by many factors like climate changes, urbanization,overgrazing, and some conservation precautions should be taken. Therefore, the target species should beknown in details. The objective of this study is to provide information about ecology, morphology, and thepopulation density of Salsola grandis which is a local endemic species from Nallihan, Ankara. It prefers clayeysaline alkaline soils with a semi-arid cold Mediterranean climate. During the field surveys between May2010 and November 2011, the morphometrical measurements of vegetative and generative organs, and theedaphic characteristics were determined. The total number of individuals of the population was calculatedas 436.612 over 48.5 × 10-4 km2. It was determined that the species has a high ratio of death, 55%, duringthe seedling period which may be the reason of the narrow distribution with the preference of specialedaphic characteristics. Keywords: Autoecology, Amaranthaceae, Halophyte, Nallihan, Salsola grandis.

Lokal Endemik Salsola grandis’ in Morfolojisi, Ekolojisi ve Koruma StatüsüÖzetTürkiye, iklim değişiklikleri, kentleşme, aşırı otlatma gibi birçok faktör tarafından tehdit edilen ve bazıkoruma önlemleri alınması gereken zengin bir biyolojik çeşitliliğe sahiptir. Bu nedenle, hedef türler ayrıntılıolarak bilinmelidir. Bu çalışmanın amacı, Nallıhan-Ankara’da lokal yayılış gösteren endemik Salsola grandis’in ekolojisi, morfolojisi ve popülasyon yoğunluğu hakkında bilgi vermektir. Bu tür, yarı-kurak soğukAkdeniz iklimi ile killi, tuzlu ve alkali toprakları tercih etmektedir. Mayıs 2010 ve Kasım 2011 tarihleriarasında arazi çalışmaları sırasında, vejetatif ve generatif organları morfometrik ölçümleri ve topraközellikleri belirlenmiştir. Populasyondaki toplam birey sayısı, 48.5 x 10-4 km2’lik yayılış alanı üzerinde436.612 olarak hesaplanmıştır. Türün yayılış alanının dar olması muhtemelen fide döneminde belirlenen %55’lik ölüm oranı ve özel toprak tercihidir.Anahtar Kelimeler: Amaranthaceae, Halofit, Nallıhan, Otekoloji, Salsola grandis.

Cınar IB, Tug GN (2015) The Morphology, Ecology, and Conservation Status of the Local Endemic SpeciesSalsola grandis. Ekoloji 24(96): 41-47.

No: 96, 2015 41

Ekoloji 24, 96, 41-47 (2015)doi: 10.5053/ekoloji.2015.17

Received: 09.04.2014 / Accepted: 20.03.2015

Inci Bahar CINAR*, Gul Nilhan TUG

Ankara University, Faculty of Science, Department of Biology, 06100, Tandogan, Ankara,TURKEY*Corresponding author: incibaharcinar@gmail.com

INTRODUCTIONThe fundamentals of species conservation are

the determination of distribution and informationabout its ecology (Heywood and Iriondo 2003). Theeffective factors of the distribution area are themacro and micro climate, characteristics of the soilson which the plants grow, habitat characteristics,and the interactions with other species(Summerhayes 1969, Currie 1991, Huntley et al.1995, Reinhammer et al. 2002, Knollová andChytry´ 2004, Pearson et al. 2004, Wotavová et al.2004, Tsiripidis et al. 2007, Landi et al. 2009, Diaci etal. 2010, Tsiftsis et al. 2012). Many endemic plantspecies have restricted distribution areas which isone of the main subjects of many ecological andphylogenetical studies (Prober and Austin 1990,Brown et al. 1996, Yucel and Altinoz 2001, Webb

and Gaston 2003). The main causes of this situationare found to be low ecological tolerance, specializedhabitat requirements, low dispersal ability, and/orlow reproduction capacity (Debussche andThompson 2003, Lavergne et al. 2004, Becker2010). Turkey has many local endemics that haveonly one distribution area, their systematics arewell-known but information about their ecology,population, and reproductive biology is not enough.For a proper and successful conservation, the targetspecies must be well-known in all details.

The Amaranthaceae family is composed of 180genera and 2500 species located all over the world,and in Turkey, it has 32 genera and 144 species.Salsola is of these genera distributed mainly inhalophytic areas. In Turkey 6 of the 20 taxa of Salsolaare endemic and one of these endemics is S. grandis

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(Yaprak 2012). S. grandis is a local endemic known only form

Nallihan and nowadays some conservation attemptshave been accomplished.

S. grandis is an annual halophytic species that itsevolution starts at the Tertiary Period and had a greatdistribution area during the Pleistocene and earlyHolocene Periods when the arid climate dominatedTurkey (Freitag et al. 1999). It was listed as criticallyendangered in the Red Data Book of Turkey (Ekimet al. 2000).

The main purpose of this study is to provide dataand information about the ecological preferences,morphological characteristics, and populationdensity of S. grandis which can provide the basicfundamentals for conservation plans.

MATERIAL AND METHODSStudy AreaThe population of S. grandis Freitag, Vural & N.

Adıgüzel (Amaranthaceae) occupies a local area at the28th km to Nallihan from Beypazari (Ankara);which is bordered by the Aladağ Mountains in thenorth, Çayırhan in the east, Nallihan in the west,and Sariyar Dam Lake, which is an important birdarea, in the south (Guner and Duman 2006). Thearea is considered with-in the borders of the Irano-Turanien phytogeographical region (Davis 1965).

Morphometric Measurements S. grandis was examined in its natural habitat

between May 2010 and November 2011. To makeall the phenological observations andmorphometrical measurements on the sameindividuals, 60 individuals were marked and thedimensions of the vegetative and generative organswere measured when they were matured; then theminimum, mean and maximum values withstandard deviation were determined.

The fruit and seed measurements wereaccomplished using a BAB stereo microscope andBAB image processing and analysis system (Bs200Pro). Measurements were accomplished withrandomly chosen 100 fruits and seeds. Theminimum, mean, and maximum values withstandard deviation were determined.

The mean weight of a fruit was determined byweighting 300 randomly chosen fruits in 6 sets. Thesame procedure was also applied for seed.

The parts of the generative organs, anther, stigmaand stylus lengths, and ovary length and width weremeasured from 10 different flowers using the BAB

stereo microscope and BAB image processing andanalysis system (Bs 200Pro).

To find out the number of seeds per individual,the terminal branch and lateral branches of 10 of themarked 60 individuals were covered with soft veil;then after ripening the number of seeds of eachbranch was counted.

Population DensityThe distribution area of the S. grandis population

was determined by GPS (GARMIN GPSMAP 62s).For determination of population density, 20quadrats of 1 m2 were randomly chosen. Thenumber of individuals at vegetative and generativestages of the species was counted and then the deathratio and population density were calculated. Thethreat category was re-evaluated according to theIUCN criteria (Anonymous 2010). If there are anyactivities at the area threatening the population, theywere also observed.

Accompanying SpeciesDuring the vegetation period from May 2010 to

November 2011, plant specimens were collectedand then identified using "Flora of Turkey and EastAegean Islands I–XI" (Davis 1965-1985, Davis 1988,Guner et al. 2000) for the determination of otherspecies living at the same area with the S. grandis.The collected specimens were prepared as aherbarium specimen and deposited in theherbarium ANK.

Soil Sampling and Analysis Soil samples were taken from the study area at

germination, flowering, and fruiting stages of S.grandis. Soil samples of 1–2 kg were taken andprepared for physical and chemical analysis. All thesoil analyses were accomplished at the "GeneralDirectorate of Agricultural Research Central Soil,Fertilizer, and Water Resources Research Institute".Soil texture was determined by the Bouyoucusmethod (1955) and the chemical analysis wereconducted according to Richards (1954).

Climate of the Distribution Area Climate of the area was determined according to

Emberger using the data of the Beypazari andNallihan meteorological stations (Akman 1999).

RESULTSThe habits, parts, and habitat of S. grandis can be

seen in Fig. 1.Morphological Characteristics of Leaf and

PlantThe measurements of plant length, leaf length

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and width, and number and length of branches,from the 60 marked individuals are as follows; meanplant length is 41.3 ± 13.5 cm. The mean leaf widthand length and bracts length are as followsrespectively; 0.4 ± 0.2 mm, 5.3 ± 1.8 mm, and2.3 ± 1.04 mm. The mean number of secondaryand tertiary branches and their mean lengths are29 ± 14 and 9 ± 7 and 9 ± 7.6 cm, and 4.6 ± 2.4cm respectively.

Morphological Characteristics of theGenerative Organs

Anthesis occurs between June and late July.Flowers are in spikes which results in a highnumber of fruits and seeds. The generative organswere measured at anthesis.

The thecas of each anther are not equal in length.The mean length of the longer theca is 1.73 ± 0.06mm and that of shorter theca is 1.70 ± 0.07 mm.The measured parts of the gynaecium and theirmean sizes are as follows: stigma length 1.19 ± 0.25mm, stylus length 1.14 ± 0.25 mm, ovary length0.70 ± 0.18 mm, ovary width 0.80 ± 0.09 mm, andpistil length 3.02 ± 0.21.

The fruits start to develop in August and theseeds mature in September and October. The meanweight and diameter of a fruit is 0.014 ± 0.0009 gand 12.39 ± 3.60 mm. The mean number of seedsproduced by an individual is 718 and the meandiameter and weight of a seed were measured as3.07 ± 0.39 mm and 0.008 ± 0.0006 g respectively.

Comparison of the Morphological Characte-ristics of the Specimens from Nature and from aGreenhouse in Kassel Germany

There were some differences between themeasurements of some parts of the plant and thedescription of S. grandis (Freitag et al. 1999) whichcan be seen in Table 1. The measurements fordescription were done with the plants grown in thegreenhouse at Kassel (Freitag et al. 1999) which maybe the cause of these differences.

Edaphic and Bioclimatological Charac-teristics of the Area

Although there are some small seasonalfluctuations, S. grandis grows over clayey soils, andprefers alkaline soils with a pH over 8.5. In the studyarea, the salinity fluctuates throughout the year andreaches the highest level during summer. Highevaporation due to the high temperatures and lowprecipitation, cause this increase. The EC of thesoils which indicates salinity were measured as 5.80

dS/m, 8.62 dS/m, and 8.46 dS/m in the spring,summer, and fall, respectively. The most dominantsoluble and exchangeable ion is Na in the area. Thephysical and chemical analysis results of the soilsamples are given in Table 2 and 3.

For the determination of the climaticcharacteristics of the study area, the climatic data oftwo closest stations, Beypazari and Nallihan, wereused and the bioclimatical analysis is summarized inTable 4. There is an arid season from May to themiddle of October at Beypazari and from April tothe middle of October at Nallihan. The area isunder the influence of Mediterranean climateaccording to the s value which is lower than 5.

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Fig. 1. The general view of S. grandis and its parts. a- General view, b- Seedling, c- Flower, d- Generative organs, e- Fruit.

Table 1. Some differences of the measurements between the authors and the description of S. grandis.

Population Density and conservationStatus and Risk Assessments

The distribution area was measured as 48512.47m2 by GPS, 20 sampling areas of 1 m2 wererandomly determined to find out the number ofindividuals, but 5 of them were lost during thestudy. The number of individuals was counted atboth seedling and fruiting periods in each samplingarea. The mean number of individuals at onesampling area at seedling and fruiting periods are asfollows 20 and 9, respectively. The number ofindividuals of overall population during the seedlingand fruiting seasons are 970.249 and 436.612respectively. These results indicated that only 45%of the individuals can reach maturity. The area is inthe borders of an important bird area but, there is nostrict conservation status.

Accompanying SpeciesSalt marsh vegetation dominates the area and the

other species accompanied with S. grandis are;Agropyron cristatum (L.) Gaertner subsp. pectinatum(Bieb.) Tzvelev var. pectinatum, Alhagi pseudoalhagi L(Boiss.) Desv., Alyssum sibiricum Wild., Anabasisaphylla L., Atriplex aucheri Moq., A. laevis C.A.Mey.,Brassica elongata Ehrh., Cardaria draba (L.) Desv.subsp draba, Cephalaria transsylvanica (L.) Schrader,Cerastium anomalum Waldst. & Kit., Crepis foetida L.subsp. foetida, Halanthium kulpianum (Koch.)Bunge., Lamium amplexiacaule L., Lepidiumgraminifolium L., L. perfoliatum L., Petrosimonianigdeensis Aellen, Reaumuria alternifolia (Lab.) Britten,Roemeria hybrida (L.) DC. subsp. hybrida, Salsolanitraria Pall., Scorzonera cana (C.A. Meyer) Hoffm.var. jacquiniana (W. Koch), Senecio vernalis Waldst. &Kit., Setaria viridis (L.) P.Beauv., Tamarix parvifloraDC., Turgenia latifolia (L.) Hoffm., Ziziphora tauricaBieb. subsp. taurica, Zygophyllum fabago L. There are26 taxa in the study area and 6 of them are endemicwith the ratio of 23.7%. The distributions of thesetaxa to the phytogeographical regions are as followsIrano–Turanien 5 (19.23%), cosmopolite andunknowns 21 (80.77%).

DISCUSSIONLocal endemics have special adaptations to their

mostly stressful restricted habitats and showdifferent morphological characteristics with theirclose relatives (Chapin et al. 1993, Poorter andGarnier 1999). In these restricted and specializedconditions (habitats), they share the area with asmall number of species and above-ground

competition is weak with sparse vegetation cover(Lavergne et al. 2004).

S. grandis shares the distribution area with 26taxa, 6 of which are endemic. But theseaccompanying taxa do not prefer to penetrate thearea where S. grandis is dense. Especially at floweringand fruiting periods, S. grandis dominates thelandscape (Fig. 2). Anabasis aphylla is the mostcompelling accompanying species which is rare inTurkey.

S. grandis grows in open habitats with sparse

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Fig. 2. Landslip after heavy rains.

Table 2. Physical properties of the soils

Table 3. Chemical properties of the soils.

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vegetation cover on saline-alkaline clayey soils. Thearea is under the influence of the semi-arid coldMediterranean climate. Nowadays, the fluctuationsin climatic conditions lead to changes in thechemical properties of the soils which are effectiveon the population density of S. grandis. Changes inclimatic conditions and edaphic factors can changethe distribution area and decrease the populationdensity which increase the risk of extinction (Fenuet al. 2011). Annual fluctuations in the environ-mental conditions can also decrease the populationdensity.

Electrical conductivity is one of the salinityindicators in soils and throughout the year fluctuatesit is always greater than 4 dS/m which means thesoils of the area are saline (Richards 1954). Thespecies completing their life cycles on saline soils arecalled as halophyte. So S. grandis is a halophyticspecies but germinates in spring when the soil

salinity decrease and avoids high salinity. In general, local endemics produce a small

number of seeds (Lavergne et al. 2004), anindividual of S. grandis produce 718 seed on theaverage. According to the germination trials, seedsare viable and easily germinate with a germinationratio of 98.3% (Ayyıldız et al. 2012). Although witha fairly high number of seeds and germination ratio,S. grandis is restricted to a small area. The area issurrounded by bare small hills without vegetationcover. The soils of the hillsides easily erodeespecially after heavy rains (Fig. 2). During thegermination period, landslip causes the burial ofseeds and seedlings, so the number of individualsdecreases. Most of the seedlings cannot reachmaturity which is the main cause of low populationdensity.

The threaten category of S. grandis was re-evaluated and found to be that there is no change,although there are some conservation attempts inthe area, it is still CR due to the fact that is knownonly in one locality and covering an area of less than100 km² (Anonymous 2010).

As other endemic and rare species, S. grandis isalso susceptible to changes in environmentalconditions, so the information acquired can providefundamental knowledge for future studies ongermination and conservation studies of S. grandis.

ACKNOWLEDGEMENTS The authors are thankful to Dr. Ahmet Emre

Yaprak, Isa Baskose, Selda Goksen, and the staffs of“General Directorate of Agricultural ResearchCentral Soil, Fertilizer, and Water ResourcesResearch Institute” for their kind help.

Table 4. The climatic analysis of the study area.

P: Mean annual precipitation (mm), M: maximum meantemperature of the hottest month (°C), m: minimum meantemperature of the coldest month (°C), PE: summer precipitation(mm), S: aridity indices (S = PE / M), Q: pluviometric quotient(Q= 2000 × P / M² – m²), Sp: spring, W: winter, F: fall, Su:summer (Emberger 1932).

REFERENCESAkman Y (1999) İklim ve Biyoiklim (Biyoiklim Metotları ve Türkiye İklimleri). Kariyer Ltd., Ankara. Anonymous (2010) Guidelines for Using the International Union for Conservation of Nature (IUCN)

Red List Categories and Criteria. Version 8.1. Prepared by the Standards and Petitions Subcommittee, Gland.Ayyıldız G, Çınar İB, Yaprak AE, Tuğ GN (2012) Salsola grandis (Chenopodiaceae) Tohumlarının

Çimlenmesi Üzerine Işık ve Tuzluluğun Etkisi. In: Vardar Y (ed), Proceedings of the 21. National BiologyCongress , 3-7 September 2012, İzmir, 562-563.

Becker T (2010) Explaining rarity of the dry grassland perennial Astragalus exscapus. Folia Geobotanica 45:303-321.

Bouyoucus GJ (1955) Hydrometer method improved for making particle size analysis. Agronomy Journal54: 464-465.

Brown JH, Stevens GC, Kaufman DM (1996) The geographic range: size, shape, boundaries, and internalstructure. Annual Review of Ecology and Systematics 27: 597-623.

Chapin FS, Autumn K, Pugnaire F (1993) Evolution of suites of traits in responseto environmental stress.American Naturalist 142: 78-92.

Currie DJ (1991) Energy and large-scale patterns of animal and plant-species richness. American Naturalist137: 27-49.

Davis PH (1965-1985) Flora of Turkey and East Aegean Islands, Vol. 1-9. Edinburgh University Press,Edinburgh.

Davis PH, Mill RR, Tan K (1988). Flora of Turkey and East Aegean Islands, Vol.10. Edinburgh UniversityPress, Edinburgh.

Debussche M, Thompson JD (2003) Habitat differentiation between two closely related Mediterraneanplant species, the endemic Cyclamen balearicum and the widespread C. repandum. Acta Oecologica 24: 35-45.

Diaci J, Rozenbergar D, Boncina A (2010) Stand dynamics of Dinaric old-growth forest in Slovenia: areindirect human influences relevant? Plant Biosystems 144: 194-201.

Ekim T, Koyuncu M, Vural M, Duman H, Aytaç Z, Adıgüzel N (2000). Türkiye Bitkileri Kırmızı Kitabı(Red Data Book of Turkish Pants). Türkiye Tabiatını Koruma Derneği ve Van Yüzüncü Yıl Üniversitesi,Ankara.

Emberger L (1932) Sur une formule climatique et ses applications en botanique. La Meteorologie, No: 92-93, Paris.

Fenu G, Mattana E, Bacchetta G (2011) Distribution, status and conservation of a Critically Endangered,extremely narrow endemic: Lamyropsis microcephala (Asteraceae) in Sardinia. Fauna and Flora InternationalOryx 45(2): 180-186.

Freitag H, Vural M, Adıgüzel N (1999) A remerkable new Salsola and Chenopodiaceae from Central Anatolia,Turkey. Willdenowia 29: 123-139.

Guner A, Ozhatay N, Ekim T, Baser HC (2000) Flora of Turkey and East Aegean Islands, vol. 11,(Supplement 2). Edinburgh University Press, Edinburgh.

Guner ED, Duman H (2006) Nallihan (Ankara) Kuş Cenneti Florası. OT Sistematik Botanik Dergisi13(2): 91-114.

Heywood HV, Iriondo MJ (2003) Plant conservation: old problems, new perspectives. BiologicalConservation 113: 321-335.

Huntley B, Berry PM, Cramer W, McDonald AP (1995) European higher plants using climate responsesurfaces. Journal of Biogeography 22: 967-1001.

Knollova I, ChytryM (2004) Oak-hornbearn of the Czech Republic: geographical and ecologicalapproaches to vegetation classification. Preslia 76: 291-311.

Landi M, Frignani F, Lazzeri C, Angiolini C (2009) Abundance of orchids on calcareous grasslands inrelation to community species, environmental, and vegetationalconditions. Russian Journal of Ecology 40: 486-494.

Lavergne S, Thompson JD, Garnier E, Debussche M (2004) The biology and ecology of narrow endemicand widespread plants: a comparative study of trait variation in 20 congeneric pairs. Oikos 107: 505-518.

Pearson RG, Dowson TP, Liu C (2004) Modelling species distributions in Britain: a hierarchical integrationof climate and land-cover data. Ecography 27: 285-298.

Poorter H, Garnier E (1999) Ecological significance of inherent variation in relative growth rate and itscomponents. In: Pugnaire FI, Valladore F (eds), Handbook of functional plant ecology, Marcel Dekker, 81-103.

Prober S, Austin MP (1990) Habitat peculiarity as a cause of rarity in Eucalyptus paliformis. Australian Journalof Ecology 16: 189-205.

Reinhammer L, Olsson EG, Sormeland E (2002) Conservation biology of an endangered grassland plantspecies, Pseudorchis albida, with some references to the closely related Alpine P. straminea (Orchidaceae).Botanical Journal of the Linnean Society 139: 47-66.

Richards LA (1954) Diagnosis and improvement of saline and alkali soils. Agricultural Handbook. No: 60,The United States Department of Agriculture, Washington DC.

Summerhayes VS (1969) Wild or chids of Britain, 2 nd ed. Collins, London.

Cinar and TugEkolo ji

No: 96, 201546

The Morphology, Ecology, and Conservation Status of the Local... Eko lo ji

No: 96, 2015 47

Tsiftsis S, Tsiripidis I, Papaioannou A (2012) Ecology of the orchid Goodyera repens in its southerndistribution limits. Plant Biosystems 146(4): 857-866.

Tsiripidis I, Bergmeier E, Dimopoulos P (2007) Geographical and ecological differentiation in Greek Fagusforest vegetation. Journal of Vegetation Science 18: 743-750.

Webb TJ, Gaston KJ (2003) On the heritability of geographic range sizes. American Naturalist 161: 553-566.

Wotavova K, Balounova Z, Kindlmann P (2004) Factors affecting persistence of terrestrial Orchids in wetmeadows and implications for their conservation in changing agricultural landscape. Biological Conservation118: 271-279.

Yaprak AE (2012) Salsola. In: Guner A, Aslan S, Ekim T, Vural M, Babaç MT (eds.). Türkiye Bitkileri Listesi(Damarlı Bitkiler), Nezahat Gokyigit Botanik Bahcesi Yayinlari, İstanbul, 28-29.

Yucel E, Altinoz N (2001). Salvia wiedemannii’nin ekolojik ozellikleri. Ekoloji 38: 9-17.