Introduction

Land use change is the primary cause and key processes of disturbances in forest ecosystem dynamics (Ewers and Didham 2006; Kobayashi and Koike 2010; Rhemtulla et al. 2009). The expansion and intensification of human uses such as anthropogenic habitat modification have strong effects on biodiversity and land cover (Sala et al. 2000). Ecological integrity has been defined as a measure of the composition, structure, and function of an ecosystem in relation to the system’s natural or historical range of variation, as well as perturbations caused by natural or anthropogenic agents of change (Parrish et al. 2003). Assessing the integrity of an ecosystem requires developing measures of the structure, composition, and function of an ecosystem as compared to reference or benchmark ecosystems (Lindenmayer and Franklin 2002; Young and Sanzone 2002).

Plant diversity indices are useful tools in quantifying vegetation properties in various habitats. Species richness is one of the most direct and simple measures (Colwell and Coddington 1994; Krebs 1999). Other measures, such as Shannon index, Simpson’s diversity and Simpson’s evenness have been also used to quantify biological diversity (Vance-Chalcraft et al. 2010; Botta-Dukat 2005). Although traditional diversity indices are relatively easy to calculate, understand and communicate and they have been applied to provide tools for long-term monitoring forest ecosystems (Lamb et al. 2009), they may give little indication of site quality. Quality is an important consideration for natural resource managers because it provides critical information for identifying unique habitats, setting conservation priorities, evaluating the efficacy of restoration measures, and monitoring trends.

Among the measures that have been developed to assess the habitat quality and conservation values of plant assemblages, Swink and Wilhelm (1979) introduced the floristic quality index (FQI). Floristic quality assessment (FQI) is a recognized technique for assessing habitat quality or condition using aspects of the plant community (Chamberlain and Ingram 2012). Especially FQI has been proposed as a tool that can: compare different sites regardless of plant community type, monitor sites over time, assess the anthropogenic impacts on an area, and ultimately, measure the ecological condition of an area (Swink and Wilhelm 1994; Lopez and Fennessy 2002). Higher values of FQI indicate greater floristic quality and ecosystem integrity. FQI is increasingly used in basic ecological and conservation research (e.g. Panzer and Schwartz 1998; Spyreas and Matthews 2006; McNicoll and Augspurger 2010).

In FQI, the quality of a plant assemblage is assessed as the ecological fidelity of its species to natural or intact habitats. This index is created to evaluate site quality based on the mean coefficient of conservatism values and the number of native species. Coefficient of conservatism or CoC values represent an index (scaled from 0 to 10) assigned to native species based on their likelihood to be found in undisturbed, remnant lands (Swink and Wilhelm 1994).

Zagros Mountains of northwestern Iran, which harbor approximately 40% of the country’s forests, are covered by open park-like forests that are mainly dominated by deciduous oak trees and subject to traditional pollarding practices to produce fodder and firewood. Conditions in this region, such as topography, shortage of rangelands and animal fodder, and lack of modernization have maintained a situation of particularly intense interaction between its people and natural resources. In Zagros forest, management practices vary locally and have been found to be unsustainable (Ghazanfari et al. 2004) in many locations. Cattle grazing in forest can have negative impacts on both overstory and understory vegetation (Brown and Boutin 2009; Mabry 2002) and farming may have several impacts on plant communities at multiple scales from habitat conversion to the introduction of invasive and non-native species. Maintaining natural diversity and species composition in habitats, which are affected by anthropogenic activities, are the main goals of ecosystem management (Roberts and Gilliam 1995), thus there is a need for well-defined measures assessing these anthropogenic effects.

In Zagros region, several studies were conducted by various methods to estimate forest integrity. Many studies have been conducted using diversity indices to investigate forest integrity. Several studies have evaluated the impacts of disturbances such as grazing, windstorms and floods on the shrub density, plant diversity and forest structure (Abasi et al. 2006; Abrari Vajari and Veis Karami 2005) and some others measured biodiversity in relation to physiographic and edaphic factors (Mirzaei et al. 2008; Pilehvar et al. 2010; Heidari et al. 2010; Haidari et al. 2012). Taft et al. (2006) performed a study at Nachusa Grasslands to assess progress in tallgrass prairie by standard diversity measures (e.g., Shannon–Weiner Index, Evenness, Species Richness) and indices developed specifically to estimate vegetation integrity (Taft et al. 2006) but in the present study assignment of CoC and FQI and comparing them to diversity indices were performed for the first time in Iran. The objectives of this study are: (1) to assign conservatism coefficient to some herbal plant species of the middle Zagros as a pilot project (2) to compare mean CoC and FQI among different land uses and with other indices such as Shannon Wiener (H′) and species richness to examine the impacts of land use on plant community composition and forest integrity. The current study was guided by three hypotheses:(1) We expected that FQI and mean CoC have a strong ability in differentiating forest integrity among three land use types, understory grazing (UG), abandoned fields (AF), and protected area (PA) (2). We expected that understory vegetation communities in disturbed (grazed and abandoned fields) forests to have more non-native and weedy generalist species than preserved forests and, (3) we expected to find a link between plant community qualities, soil physiochemical properties and floristic quality index.

Study area

We conducted this study in Kakareza forest Watershed in Lorestan Province at Zagros forest of Iran. The study area elevation ranged from 1200 to 2400 m above sea-level. This region has a semiarid Mediterranean climate with a mean annual precipitation of 450 mm and monthly mean temperatures in January and July of −10 and 36 °C, respectively. The soil type is loam. The natural vegetation of the area consists of the relatively pure oak stands dominated by Persian oak (i.e. Quercus brantii), other companion tree species are Acer monspessulanum, Cerasus microcarpa, and Crataegus meyeri.

Kakareza forest is an ideal setting to study herbaceous layer response to human disturbance because both natural and anthropogenic disturbances have altered forest composition. Farming and grazing are the most important land uses in this region, where the majority of forest cover has been removed. The selection of the study sites was based on actual data, representing different classes and intensities of human-induced disturbance regimes. For the purposes of this study, vegetation surveys were performed in three lands uses: natural forest with Understory Grazing (UG), natural forest with Abandoned Fields (AF), and Protected Area (PA).

Sites description

UG land use has been grazed by cattle’s (mostly sheep) within the past 30 years, with no other recent forest management. Grazing in remnant forests can cause soil compaction, resulting in drier conditions, which also shifts species composition towards exotic and weedy native species.

AF land use abandoned for almost 20 years. During 1972–2009 about 353,000 ha (69%) of Zagros Forests (western Iran) are declined mainly due to converting to agricultural lands (Henareh Khalyani et al. 2012) and subsequently subjected to inappropriate tillage practices, soil disturbance and permeability.

Among these, PA forest with known and/or documented history of minimal human disturbance is characterized by an herbaceous layer with a diverse suite of native perennials, many of which are forest specialists. Preserved forests were owned by government conservation organizations, and were not actively managed for timber harvest or subject to grazing within the most recent 15 years. Vegetation types and floristic composition of all land uses were the same and only management practices were significantly different among them.

Vegetation sampling

Sampling was performed during late April to early of July 2015 to ensure that in the peak annual growth, the highest number of vascular plant species could be identified (DeKeyser et al. 2009). Of course some plant species may miss during this period and some may appear, so we surveyed plots twice to find new species to species composition. A random sampling design was used to determine the location of the plots. A total of 19 plots (7 from UG, 6 from AF and 6 from PA) were surveyed. Species presence/absence was recorded within plots of 250 m2 (Fig. 1). In each quadrat, all vascular plant species were identified to the lowest taxonomic division possible. Presence and canopy foliar cover of all species were visually estimated within each ten subplots of 0.25 m2 (Abrams and Hulbert 1987). If a plant species could not be identified in the field, it was collected, pressed, and identified in the laboratory. Presence/absence and cover data were used to calculate diversity indices.

Fig. 1
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Locations of the sampling point on the different land uses, Lorestan. Iran

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Fig. 2
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Number of taxa within each CoC category 1 (CoC 1–3), 2 (CoC 4–6), 3 (CoC 7–8), 4 (CoC 9–10) for UG, AF and PA land uses. Most taxa were assigned coefficients in the mid- to high-portion of the ranking scale for Kakareza native taxa

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Vegetation metrics

Species richness (S), (Magurran 1988), species diversity indices including Menhinick, Margalef, Shannon Wiener (H′), Simpson’s diversity index (Simpson 1949) and Fisher α index and mean species percent cover were calculated for different land uses.

Soil sampling

Within each plot, we collected a composed sample of soil consisting of five systematically distributed subsamples from the upper layer of soil (0–10 cm depth) since major alterations have occurred in this horizon after the land use change (Sims 2000). Large roots and pieces of organic material, such as twigs and leaves, were removed by hand in the field. After collection, each composed sample was placed in a labeled ziploc bag that was immediately sealed, then air-dried for subsequent analyses. A sub-sample of the air-dried soil was passed through a 2 mm sieve to remove large rocks and organic debris and used for chemical analysis. pH was measured in a soil/water ratio 1:1 (McLean 1982). Soil organic carbon was determined by the Walkley–Black dichromate oxidation procedure (Nelson and Sommers 1982). Total N was measured by the Kjeldahl procedure and total phosphorus (P) was determined according to Olsen and Sommers (1982).

Assignment of CoC values

Upon identification of all collected species, a Coefficient of Conservatism (CoC) was assigned to each species. The CoC values are determined as follows in Table 1 (Taft et al. 2006; Bernthal et al. 2003; Andreas et al. 2004; Fennessy et al. 2001). We convened a committee of the most experienced botanists of Iran. Regional coefficient values were assigned a rank on a scale of 0–10. A core team of botanists met to assign a CoC value for each native species using the above-mentioned criteria. Non-natives were assigned a zero (Spyreas et al. 2012). The team consisted of Valiolah Mozaffarian, Ali Akbar Maassoumi, Mostafa Assadi, Younes Asri, Farideh Attar and Gholam Hassan Veiskarami. Supplementary data were used to verify the field experience. Flora Iranica (Rechinger 1967–1998), Color Flora of Iran (1991–2000), Dictionary of Iranian Plant Names (Mozaffarian 2004), Flora of Iraq (Townsend et al. 1985), and Biodiversity of plant species in Iran (Ghahraman and Attar 1999) provided information on range occurrences, habitat descriptions, and species nativity and rarity.

Table 1 Assignment of Coefficient of Conservatism (CoC) scores to the vascular flora of middle Zagros forest (Kakareza forest)
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Mean coefficient of conservatism

The mean CoC value was calculated by summing the CoC values of all native species and dividing by the total number of species (species richness = N): Mean CoC = ΣCoC/N.

Floristic quality index

The FQI represents a weighted estimate of species richness (N), obtained by multiplying the mean coefficient of conservatism by the square root of species richness:

$$FQI_{std}:\,mean\,CC \times \sqrt {{\text{N}}_{native} }.$$

where CoCi is the coefficient of conservatism for species i and Nnative species is the total number of native species within the area of interest (sampling site).

Modified floristic quality index

The modified FQI (FQImod) is calculated for different land uses, using the following equations:

$${\text{FQI}}_{\bmod } {:} \, \left( {\sum \left( {{\text{cover}}_{i} \times {\text{CoC}}_{i} } \right)/100} \right) \times 10$$

where coveri is the percent cover for species i at a sample unit within a sample site and CoCi is coefficient of conservatism for species (Cretini et al. 2012).

The multiscale modified Whittaker plots (Stohlgren et al. 1995; Barnett et al. 2003) were used, which have been shown to record greater species richness than some alternative sampling designs. According to Stohlgren et al. (1997a, b) and previous study in this region Pilehvar et al. (2010) the dimensions of the modified multi-scale Whittaker plots and sub-plots are shrunken to half, therefore, our sampling plots consist of a 10 m × 25 m plot (250 m2) that contains 10, 0.25 m2 subplots, 6 of them located inside plot perimeter and four of them outside the perimeter of 25 m2 subplot, 2, 2.5 m2 subplots (in opposite corners), and 1, 25 m2 subplot (in plot center), (Barnett et al. 2003).

Statistical analyses

The mean values of species cover and calculated indices were compared by means of an analysis of variance (ANOVA). Before performing the ANOVA, we tested the normality and homoscedasticity assumptions with Kolmogorof-Smirnov and Levene’s tests, respectively. The LSD procedure was used to separate the means of the plant diversity indices that differed at p ≤ 0.05. Statistical processing was performed using SPSS 16 Software.

Results

A total of 194 vascular plant species were recorded in 19 plots, which belonged to Papilionaceae (36 species), Composita (24 species), Poaceae (19 species), Brassicaceae (16 species), Apiaceae (15 species), and other families (78 species).

Common diversity indices (Margalef, Menhinic, Shannon, Simpson and Fisher α) were higher in AF land use. Shannon’s diversity and Simpson diversity index for all species showed no significant difference among different land uses. Fisher α diversity index, Margalef and Menhinic showed significant difference among three land uses (Table 2; Fig. 3).

Table 2 Mean values of plant diversity and ANOVA results (F), in middle Zagros forest (Kakareza forest)
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Fig. 3
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Mean of Menhinic, Margalef and Fisher indices at three land uses, significant differences denote at α 0.05 using LSD post hoc test

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Coefficient of conservatism and floristic quality index

We assigned coefficients of conservatism to 128 native taxa identified in three land uses. Non-native species were all assigned a CoC score of 0. Results showed that the second category of CoC (CoC 4–6) had the greatest abundance in three land uses (Fig. 2).

There were 88 native plant species in PA, while 81 native plants were found in two other land use types (i.e. AF and UG). PA land use had greater richness of native, mean CoC value and higher FQI than UG and AF land uses.

The difference of the mean CoC-values between AF and PA may not be great (0.58), but it does appear that mean CoC scores calculated using PA CoC values are consistently greater than Mean CoC scores calculated using AF CoC values. The greatest difference of FQI was between PA and AF (6.95) while AF and UG showed the lowest difference (2.0). For the AF land use, FQImod score was higher than FQI score (Table 3), due to the mean sum of species cover was higher (49.86) in AF land use. Totally, in the AF land use, the cover of species belonging to the first and second CoC categories was 93.86% of the total area, while, in the UG and PA land uses, this species cover was 91.77 and 90.44%, respectively.

Table 3 Summary of floristic quality variables for UG, AF and PA land uses
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Soil chemical and physical analyses

Results indicated that there were differences in soil physiochemical traits associated with the different land uses (Table 4; Fig. 4). Soils under different land uses differed markedly in some of their properties. Soils under PA showed the highest organic carbon, nitrogen and pH. Available phosphorus and clay content were the highest in UG, which decreased in AF and PA. Soil C:N ratios for the top 10 cm were not significantly different among land uses, whereas, the C:N ratio and available potassium were the highest in the AF land use (Table 4).

Table 4 Result of soil physiochemical traits in sites under different land uses in middle Zagros, Iran
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Fig. 4
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Mean of organic carbon, Nitrogen and Silt content at three land uses, significant differences denote at α 0.05 using LSD post hoc test

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Discussion

The most important aspect of this study is assigning Coefficient of Conservatism (CoC) score to the middle Zagros forest of Iran for the first time. Although the concept of conservatism coefficient was introduced for the first time in Iran, botanical experts welcomed this idea and after numerous meetings, conservatism coefficient was assigned to the plant species in the middle Zagros forest. The study results highlighted the differences between the application of common diversity indices and mean CoC and FQI in ecosystem integrity in different land uses. In general, human disturbance in grazing and abandoned fields had great impacts on herbaceous species community quality.

We expected that excluding anthropogenic disturbances from PA by protection management leads to different vegetation compositions and enhanced ecosystem stability, and observed that biodiversity indices had the highest values in AF land use. We observed a decrease in total diversity and total richness in the PA land use, but there was corresponding increase in mean CoC value and FQI in this land use. We observed high floristic quality and high mean CoC, at a site with minimal human disturbance (PA) and low floristic quality or low mean CoC at a site with a high degree of human disturbance (AF). Our results were in agreement with the study of Gerken Golay (2013) that showed that mean CoC was the highest for preserved area and lowest for secondary forest sites in Iowa forests.

Researchers have argued that one of the problems with diversity measures is the equal weighting of every species regardless of its tolerance to disturbance or its fidelity to a specific habitat (Wilhelm and Masters 1995). Despite differences among the land uses, the fail of Shannon and Simpson diversity indices to demonstrate the differences in the different land uses is one of the weaknesses of diversity indices so that these indices could not identify subtle compositional shifts that are important for conservationists (Rooney and Rogers 2002; Cohen et al. 2004; Hooper et al. 2005; Filippi-Codaccioni et al. 2010; Cretini et al. 2012) and do not indicate whether inherent characteristics of a species lead to greater vulnerability to disturbance. Finally, these measures provide little information on site quality. The high values of richness indices in the AF land uses were also unexpected and it is another weakness of diversity indices.

The results indicated that FQI can be helpful to compare the floristic quality among different land uses and can identify the best land use with high floristic composition. Mean CoC and FQI aggregate more qualitative information on individual species and overall community composition could be useful to assess factors such as conditions of natural areas, their conservation value and impact of human disturbance better (Noss 1990; Lavorel and Garnier 2002). The higher values of diversity indices in the AF land use have been addressed to a short-term response of the system to disturbance, as emphasized by Pitkänen (2000), Peltzer et al. (2000) and Roberts and Zhu (2002). This result is also in agreement with other studies by Odum (1985), as well as Sheil and Burslem (2003) who expressed that species diversity often increases in response to disturbances. However, these results are in contrast with the studies by Findlay and Houlahan (1997), Mensing et al. (1998), Smith and Haukos (2002) who declared that the vegetation diversity has been found to be negatively correlated with increased agriculture and urban land use in wetland.

Clearly, the significant decrease in mean CoC and FQI in the AF land use can be explained by the presence of low conservative species, loss of high quality indicator species, and/or a reduction or loss of native species. Decrease in tree layer density and configuring open area in coppice Zagros oak forest, is an opportunity for exotic species invasion; since exotic species compete with native species for resources (Olff and Ritchie 1998). Bromus. dantonieh in Bromus tectorom , Trifolium stellatum, Trifolium arvense, Trifolium campestre, Euphorbia sororia are widespread species that are known to be disturbance tolerant and abundant in the AF land use. These plants have low CoC values (first CoC category) and are considered as good indicators of habitat conditions. The least conservative species (CoC values < 3) are adapted to extreme anthropogenic or natural degradation that eliminates both high and mid conservatives (Freyman et al. 2015).

In turn, Astragalus leonardii, Astragalus longirostratus, Ranunculus pinardi, Vaccaria grandiflora, Gypsophila persica, Bongardia chrysogonum, Nigella oxypetala and Dactylis glomerata are not tolerant of disturbances and they were observed in only the PA land use. Thus, these species appear to be good indicators of high ecological integrity in Zagros forest. Since these are sensitive species and might become absent quickly after disturbances and they can be a good predictor of the health of the system as they are either present or absent when management changes (Cousins et al. 2004).

Pietrzykowski (2014) expresses that many plant species are good indicators of habitat conditions. The more endemic and narrowly distributed species that exist in an area, the higher the floristic quality of the area should be. On the other hand, if widely distributed species constitute the main body of a flora, the floristic quality will be obviously low (Tu et al. 2009). These results highlight the subjective nature of CoC-value assignment and emphasize on the fact that plants in PA are more “conservative”.

In contrast to FQI, that was a reliable indicator to assess protection practices, FQImod lacks the ability for proper judgment on vegetation integrity in the PA land use. As the result of Zagros degradation and increases in the distance between trees, the absorbed irradiance by ground flora has been increased and this condition leads to the dominance and expansion of less conservative taxa and disturbance tolerant species (i.e., CoC scores of 1–6). Therefore, in AF land use, percent cover was the highest value. These species are often opportunist, invasive and weedy plants. More disturbance tolerant species with greater percent cover increased the modified floristic quality index in AF over PA, which had more conservative species and lower percent cover. Some studies in Central Europe also have shown that the reduction of the cover of dominant species is due to disturbance (Wohlgemuth et al. 2002). PA land use has higher floristic quality and it is a healthy land use compared to UG and AF land uses. Among the indices tested in this study, the Mean CoC and FQI would be the most sensitive ones in detecting changes in the forest integrity result of Zagros forest. We realized that the modified FQI alone will not describe forest integrity and it must be complemented by indices such as FQI and mean CoC.

Forest integrity and soil physiochemical properties linkage

There were differences in physiochemical soil properties in three land uses. Vegetation cover has fundamental effects on soil properties (Rutigliano et al. 2004), mainly due to its contribution of organic matter to soil.

Our study showed that soil organic C, available N, and available K generally decreased with increases in disturbances, whereas, available phosphorus and pH tended to increase. These results may be attributed to the frequent disturbance of these soils by occasionally removing rock fragments. The impacts of farming on soil organic carbon are well documented, with a significant reduction in soil organic carbon (Collins et al. 2000; Post and Kwon 2000). Cultivation in Zagros forests, which is mainly located on steep slopes leads to surface soil erosion and nutrient loss. Soil recovery after cultivation abandonment occurs slowly and pioneer plant species that are mainly invasive species occupy these fields. The primary stages of secondary succession involve similar conditions, but are not sustained. Organic matter has key influence on physical, chemical and biological soil attributes. Thus, soil physiochemical properties can be a good indicator of soil health and forest integrity. This result was consistent with the study by Wu et al. (2010) who reported that the accumulation of SOC was greater in natural grassland than in arable land in the southern Loess Plateau. Wang et al. (2007) concluded that SOC content in woodlands and grasslands decreased after cultivation in the central Loess Plateau. In contrast, Schiffman and Johnson (1988) found no difference in total soil C among converted plantations, old field afforested sites, native forests and control fields.

The cessation of cultivation and conversion to perennial vegetation will increase total soil carbon (Degryze et al. 2004). AF land use had higher amounts of K as compared to the UG and PA land uses, which may be due to the addition of K-fertilizers. This result is in accordance with Kosmas et al. (2000) in Greece forests. Similar trends for potassium were found for exchangeable sodium. Due to soil quality would appear to be an ideal indicator of sustainable land management (Herrick 2000), we can state that the increases in Floristic quality values and soil organic carbon in the protected site revealed that protection management is likely successful during a fifteen-year period and the conservation of vegetation on PA land use led to the sequestration of soil organic carbon.

Conclusion

The results of the study indicated that CoC and FQIs could better discriminate land use integrity than species diversity indices such as Simpsons or Shannon. The ability of the CoC and FQI to detect differences helps ecologists and managers to assess the protection practices. Land managers could identify areas that support a large proportion of native and high conservative flora. The integration of the diversity indices with the FQI could be considered as a valid methodology to assess forest integrity better and more research should be conducted using the FQI and related metrics on natural and disturbed ecosystems to determine whether restoration and mitigation projects can attain the goals of achieving natural ecosystem functions.