Species co-occurence in coastal dunes in North of Turkey
Senay Ulu Agır1•Hamdi Guray Kutbay1• Burak Surmen2Received: 1 April 2016 / Accepted: 5 August 2016 / Published online: 30 August 2016 Ó Accademia Nazionale dei Lincei 2016
Abstract Plant co-occurence patterns were studied in coastal dunes in Central Black Sea Region of Turkey (North of Turkey) by the help of the checkerboard score (C-score), and the checkerboard score for abundance data (CA-score) along climatic and local gradients. There were significant differences along the local and climatic gradi-ents with respect to both standardised C- and CA-scores. Standardised C-scores were found to be significantly dif-ferent along sea–inland gradient except for fixed dune zone, while standardised CA-scores were significantly different in embryonic and main dune zones. Our results were supported HBR (humped-back relationships) hypothesis in studied coastal dunes because standardised scores were usually found to be [0. In other words, seg-regation was prevailed in studied species rather than aggregation.
Keywords Central Black Sea Region Coastal sand dunes Humped-back relationships (HBR) hypothesis Species aggregation Species seggregation Stress-gradient (SGH) hypothesis
1 Introduction
Coastal dunes are stressful habitats and characterized by close relationships between abiotic and biotic factors. Plant communities in coastal dunes changed along a gradient from the shoreline to the inland regions, resulting in a characteristic zonation of plant communities (Isermann
2011; Lane et al. 2008; Agır et al. 2014). The most sig-nificant stress factors are salt spray, sand burial, substrate instability, and nutrient limitations, etc. (Maun2009; Agır et al. 2014; Ruocco et al.2014). Inter- and intra-specific relationships may be very different and habitat properties may greatly change even at local scales (Maestre et al.
2009; Maltez-Mouro et al.2010; Santoro et al. 2012). It has been emphasized that species interactions are considered determinants of community diversity, with competition thought to play leading roles in community organization (Rey et al.2016). There were two hypothesis regarding competition and facilitation along gradients of environmental severity especially in harsh environments like coastal dune ecosystems. The first hypothesis is known as ‘‘stress-gradient hypothesis (SGH)’’ primarily described by Bertness and Callaway (1994). This hypothesis is a general conceptual model predicting that the relative fre-quency of facilitation and competition will vary inversely across gradients of physical stress or ecosystem produc-tivity (Maestre et al. 2009). The second hypothesis is described by Grime (1973) and known as ‘‘humped-back relationship (HBR)’’. The HBR hypothesis suggested that under high environmental severity, the effects of facilita-tion are reduced and species richness declines as only stress-tolerant species are able to persist (Bowker et al.
2010; Vaz et al.2015). Ecosystem productivity is strongly linked with environmental/climatic factors and determines macro ecological and local gradients in species richness.
& Burak Surmen
buraksurmen@gmail.com Senay Ulu Agır senay.ulu@hotmail.com Hamdi Guray Kutbay hguray@omu.edu.tr
1 Department of Biology, Faculty of Arts and Sciences,
University of Ondokuz Mayıs, Kurupelit, 55139 Samsun, Turkey
2 Department of Biology, Kamil Ozdag Science Faculty,
Karamanoglu Mehmetbey University, 70200 Karaman, Turkey
Grime’s hypothesis is an important conceptual advance that merged the effects of productivity (or environmental stress) and species interactions (primarily through compe-tition) on species diversity (Rey et al.2016).
Coastal dunes in Central Black Sea region of Turkey (north of Turkey) cover a relatively wide area (149 km). These dunes include main dune zones (upper beach or drift line, embryonic dune, main dune, transitional and fixed dune). It has been stated that an environmental gradient occurred in coastal dunes from seaside to the inland (Prisco et al. 2013). It has been demonstrated that a gradient of stress and disturbance very closely related to distance from the sea. Sea–inland gradient is a good proxy for abiotic stress (Castanho et al.2012).
There were several studies on the prevalence of HBR and SGH in stressful environments like coastal dunes (Maltez-Mouro et al.2010; Holmgren and Scheffer2010). Bowker et al. (2010) hypothesize that because a greater number of species interactions are possible under low stress conditions and this may render intransitivity dominant over niche segregation and expansion, and resulted in positive effects of competition on species richness in low stress situations. Vaz et al. (2015) found segregation patterns for co-occurring of coastal dune species at the local scale, and segregation patterns suggested that plant communities were mainly determined by environmental heterogeneity, at the local scale. Coastal sand dunes are subjected to several disturbance factors such as sand extraction for building, presence of drainage channels and barriers, illegal urban-ism, agricultural activities and extensive hunting in Central Black Sea region of Turkey (Agır et al.2014). The eval-uation of HBR vs SGH hypotheses in coastal dune species in Central Black Sea region of Turkey may be helpful to show whether the species are selected aggregation or seg-regation along regional and local gradients by using pres-ence/absence data. The aim of this study is to evaluate which hypothesis is expected to prevail in a coastal dune ecosystem occurred in Central Black Sea region of Turkey, in the north of Turkey along regional (climatic) and local (sea–inland) gradients.
2 Materials and methods
The study area includes coastal line between Alac¸am and Terme provinces (41°2902700N and 36°3301200E) in western and eastern part of Central Black Sea region of Turkey. The study area covers a 149 km area (Fig.1). The main properties of studied localities were presented in Agır et al. (2016). There were evident climatic differences between the western and eastern part of the study area. Mediter-ranean climate is widespread in the western part of the study area, while oceanic climate is widespread in the
eastern part (Yalcin et al. 2011; Agır et al. 2014). As a result of this a climatic gradient is formed from western to the eastern part of the study area (Table1).
2.1 Sampling
Eight transects from seashore to the inner land included five main zones namely upper beach or drift line, embry-onic dune, main dune, transitional and fixed dunes. Tran-sects were orthogonal to the seashore and varied from 25 to 700 m depending on dune morphology and on the length of the natural vegetation strip. Transects were used for better characterize of climatic and local gradients from seashore to inland. A total number of 327 sampling units were considered and cover-abundance values were determined in contiguous 2 9 2 m square areas (Acosta et al. 2000). Braun–Blanquet vegetation classification method (Mueller-Dombois and Ellenberg1974) was used to estimate cover-abundance values based on the following percentages: 0, 1, 1–5, 5–10, 10–25, 25–50, 50–75 and 75–100. Relative plant coverage was estimated visually in each unit (Cakan et al. 2011). Cover-abundance values were converted to van der Maarel’s cover-abundance values as: 1 %, 1; 1–5 %, 2; 5–10 %, 3; 10–25 %, 5; 25–50 %, 7; 50–75 %, 8 and 75–100 %, 9 (Hill1979).
2.2 Statistical analysis
ECOSIM 7 software (Gotelli and Entsminger 2004) was used to evaluate co-occurrence patterns by the help of null model analyses and the numbers of areas (k) were taken into account in each case. The first step consisted of the analysis of co-occurrence patterns for the whole study area, considering the whole data set (k = 1, total area). Second step is related to the analysis of co-occurrence patterns along the climatic gradient by considering patterns of co-occurrence at each site and comparing them across the seven sites (k = 7 sites). Finally, third step is related to the analysis of co-occurrence patterns along the local (sea– inland) gradient, and co-occurrence patterns in each habitat type and comparing these patterns across the five habitat types (Vaz et al. 2015).
2.3 Statistical analyses of co-occurrence patterns
Patterns of co-occurrence were assessed from both pres-ence/absence and abundance data matrices, where each row or column represented a given species or analysis unit, respectively. The checkerboard score for abundance data (CA-scores) were calculated (Ulrich and Gotelli2010). In the first step of analysis, a matrix with 92 species by 32 analysis units was considered for the whole study area. 32 analysis units consist of typical dune zones (driftline,
embryonic or primary zone, main dune zone transitional dune zone and fixed dune zone). In four localities (Doyran, Sahilkent, Cernek and Cobanyatagı) all zones are present, while in three localities (Costal, Hu¨rriyet and Sindel) fixed dune zone is lost. In summary, 20 analysis units (5 zones 9 4 localities) are present in four localities, 12 analysis units (4 zones 9 3 localities) are present in three localities and total 32 units are present in whole study area while C- and CA-scores were calculated for each pair of species. For presence/absence data, C-scores were calcu-lated from the following equation:
C score ¼ Rð i SÞ Rj S
;
where Ri and Rj refer to the row totals (where each row represents a given species) for species i and j, respectively, and S refers to the number of matrix squares where both species occur (Gotelli2000). The CA-scores were calcu-lated from the following equation:
CA score ¼ 4CA=R R 1ð Þ C C 1ð Þ;
where R and C are the number of rows and columns of the matrix, respectively. Null matrices were generated using a ‘‘fixed rows-fixed columns’’ model which keeps constant both the species number and frequency. The indices obtained from each matrix were compared with null matrices (10.000 randomly assembled matrices) (Maltez-Mouro et al. 2010), and the data were implemented in ECOSIM 7.0 software by calculation of CA-score and row/column abundances were re-sampled by the help of fixed null models (Gotelli2000; Ulrich and Gotelli 2010; Vaz et al.2015).
Values for standardized scores higher or lower than 0 indicated prevailing spatial segregation or aggregation among the species within a community, respectively (Gotelli and McCabe 2002; Maltez-Mouro et al. 2010; Gotzenberger et al. 2012; Vaz et al. 2015). C- and CA-scores were compared by the help of one-way ANOVA using a SPSS (21.0 version) software (IBM Corporation
2012).
Fig. 1 Studied localities in coastal dunes in North of Turkey
Table 1 Climatic properties of
the study area Western part Eastern part
The mean annual precipitation (mm) 672.4 922.1 The mean annual temperature (°C) 13.5 15.1
Index of xericity (S¼ PE=M) 3.4 5.49
The pluviometric quotient 85.4 121.3
Life forms of the studied species were determined according to Ellenberg and Mueller-Dombois (1967).
3 Results
It has been found that dominant life form was therophytes in all zones. It was followed by hemicryptophytes (Fig.2). There were significant differences along the regional (climatic) gradient with respect to both standardized C- and CA-scores. All of the studied localities were significantly different regarding C-scores along the climatic gradient except for Hu¨rriyet and Sindel localities. CA-scores were also significantly different except for Sahilkent, Hu¨rriyet, Sindel and Cobanyatagı localities. The highest standard-ized C- and CA-scores were found for Cernek, and Costal localities, respectively. However, the lowest standardized C and CA-scores were found in Hu¨rriyet locality. Stan-dardized scores were usually found to be [0. CA-scores were found to be \0 in Hu¨rriyet locality along climatic gradient, but it was not statistically significant (Figs.3,4). Standardized C-scores were significantly different along local (sea–inland) gradient except for fixed dune zone. Standardized CA-scores were significantly different in embryonic and main dune zones. However, these scores were not significantly different in other zones. The highest standardized C-scores were found for fixed dunes although C-scores in fixed dunes were not significant, while the highest standardized CA-scores were found for embryonic dunes along the seashore–inland gradient. The lowest
standardized C- and CA-scores were found in main and drift line, respectively (Figs.5,6).
4 Discussion
Bertness and Callaway (1994) stated that species aggre-gation and facilitation is very widespread in harsh envi-ronments like coastal dunes. Forey et al. (2009) also supported SGH and they found both positive to negative associations between plant species along French coastal sand dunes. However, several researchers cannot be found a clear evidence for SGH. For example, Castanho et al. (2015) did not find a clear evidence for facilitation in coastal dune ecosystems. Maltez-Mouro et al. (2010) found SGH is only partially true and co-occurrence patterns were dependent on the spatial scale. As further from drift line, the combination of intermediate levels of stress and dis-turbance promotes complex variations of environmental conditions at fine scales (Lomba et al.2008). This is also linked to the environmental heterogeneity of the study area along climatic and local gradients with several habitats being considered from drift line to inland (Carboni et al.
2011). Michalet et al. (2006) and Holmgren and Scheffer (2010) have developed a different standpoint for HBR and they stated that only stress-tolerant species are able to persist in harsh environments and facilitation is decreased under such conditions. Vaz et al. (2015) emphasized that plant co-occurrence types in coastal dune ecosystems may be changed over temporal and spatial scales at the whole community level in harsh conditions.
Several authors suggested that species segregation is prevalent along sea–inland gradient (Armas and Pugnaire
2009; Santoro et al. 2012). They also emphasized that the species in embryonic dunes and inland dunes have a ten-dency for species aggregation. Our data were not supported aggregation, because C- and CA-scores were found to be [0 along local (sea–inland) gradient in coastal dunes of Central Black Sea region and agree with HBR rather than SGH (Vaz et al. 2015). CA-scores were only found to be \0 in Hu¨rriyet locality and this could be attributed to species aggregation according to several authors (Maestre et al. 2009; Santoro et al. 2012). Both C- and CA-scores were not significant in Sindel and CA-scores were not significant in Cobanyatagı. The lowest C and CA-scores were found in Hu¨rriyet locality. In all localities disturbance is widespread. However, disturbance factors are more prominent in Hu¨rriyet and Cobanyatagı localities. For example, in Hu¨rriyet locality, vegetation was severely disturbed due to Pinus pinaster Aiton subsp. pinaster plantations in transitional zone and this zone was mixed with main dune zone in Hu¨rriyet locality. Miller (2015) stated even small changes in main and transitional dune
CH
8%
G
10%
H
30%
P
6%
PL
2%
T
44%
Fig. 2 Percentage distribution of life forms all studied localities (T therophyte, H hemicryptophyte, G geophyte, CH chamaephyte, P phanerophyte, PL phanerophytic liana)
zones may have greater effects than any other dune habitat, which also makes interdunes particularly susceptible to flooding. Inundation is also an important disturbance factor
in drift line in Hu¨rriyet. In fixed dunes, Sophora alopecu-rioides L. var. alopecualopecu-rioides is widespread in Hu¨rriyet locality and is very resistant to the negative effects of
Fig. 3 Standardized C-scores calculated for each locality
Fig. 4 Standardized CA-scores calculated for each locality
inundation (Agır et al.2016). However, the negative CA-scores could be neglected because they were not statisti-cally significant. Vaz et al. (2015) emphasized that climatic gradient had only a minor effect on plant community
structure. Inundation is also found almost all zones in Cobanyatagı and as a result of inundation the species in drift line extended to inner zones. It has been known that inundation has a pronounced regulatory effect on the
Fig. 5 Standardized C-scores calculated for each habitat type (a upper beach and drift line dunes, b embryonic dunes, c main dunes, d transitional dunes, e fixed dunes)
Fig. 6 Standardized CA-scores calculated for each habitat type (a upper beach and drift line dunes, b embryonic dunes, c main dunes, d transitional dunes, e fixed dunes)
distribution and abundance of plant species (Deegan and Harrington 2004). The highest CA-scores were found in embryonic dunes. Honrado et al. (2010) and Waugh and Aarssen (2011) found that this may probably be indicated heterogeneity of species composition in embryonic dunes and this is the result of combined effect of local gradients and niche differentiation by plant species and related to differences in coastal dynamics. The prevalence of spatial segregation is also an indicative of competition among the species within a community (Maltez-Mouro et al. 2010). Costa et al. (2009) and Macedo et al. (2010) developed an alternative model for HBR and they have been suggested that facilitation is widely reduced in stressful conditions and only stress-tolerant species are able to persist in such harsh conditions and species aggregation is shifted to species segregation as a result of high inter- and intra-specific competition (Michalet et al.2006).
Therophytes were found to be dominant life form in the study area and they were very tolerant to stressful condi-tions. The variation in the spatial association with the life form may be a result of differences in stress tolerance and the competitive responses of different life forms, since the trade-off between these traits is of great importance to the net outcome of plant interactions (Castanho et al.2012).
5 Conclusions
All of the studied localities were significantly different regarding C-scores along the climatic gradient except for Hu¨rriyet and Sindel localities. CA-scores were also sig-nificantly different except for Sahilkent, Hu¨rriyet, Sindel and Cobanyatagı localities. Standardized C-scores were significantly different along sea–inland gradient except for fixed dune zone. Standardized CA-scores were signifi-cantly different in embryonic and main dune zones. However, these scores were not significantly different in other zones. Standardized scores were usually found to be [0. CA-scores were found to be \0 in Hu¨rriyet locality along climatic gradient, but it was not statistically signifi-cant. Based on standardized scores it has been found that species segregation is prevailed in the study area.
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