Anthropic Effects on the Biodiversity of the Habitats of Ferula gummosa

Abstract

The uncontrolled exploitation of soil and plants by people has generated important ecological imbalances all over the world. This manuscript focuses its attention on the ecosystem of Ferula gummosa (FG). FG belongs to the Apiaceae family and has a vast distribution from central Asia to South Africa, as well as northwest Iran, including the Zanjan Province. This plant has diverse applications across industrial, forage and medicinal fields. To investigate the effective factors on the FG distribution, four main natural habitats were selected based on field visits and a literature review. Then, environmental factors, such as climate features, topography conditions, and soil characteristics, were collected and analysed. According to the results, the slope is mainly north-northeast with a slope of 55 to 70 degrees, and an elevation range above 2200 m is suitable for the growth of FG in the Zanjan Province. The main companion plants were Silene bupleuroides L. and Thymus kotschyanus. The results show that in the habitats where FG grew, the soil was mostly shallow, sometimes semi-deep and consisting mainly of loam, loamy sand, loamy clay and mostly clay loam with very low salinity (less than 0.7 dS/m), and was in the neutral range of soil acidity (6.9 to 7.33). Soil organic carbon was relatively high, but the amount of nutrients, such as phosphorus and potassium, was less than optimal in these soils. Next, using a Geographic Information System (GIS), maps of homogeneous areas for possible FG establishment across the province were created. In conclusion, the main factors affecting the FG distribution in the Zanjan Province were land use conversion, harvesting fodder and grazing livestock, improper exploitation of rangelands, pests and diseases of Ferula gummosa in the region. The ecological data collected on FG may be useful to understand how human action can affect the existence and extinction of many plant species.

1. Introduction

Ferula gummosa (FG) is named Barijeh, Balijeh, Ghasni and Barzard in Persian [1,2]. It belongs to the Ferula genus in the family Apiaceae. This family with at least 112 genera contains aromatic plants with hollow stems and umbrella inflorescences [3]. The genus Ferula contains 170 species and is extensively distributed from Central Asia to South Africa [4]. FG is one of the industrial, medicinal and forage valuable assets in Iran. As a dominant or associated species, it forms a wide range of plant types in mountainous areas [5]. The phenological stages of the FG plant are as follows: seed germination starts from late March to early April, and vegetative growth begins from the second half of April and continues until the first half of July. According to the monocarpic nature of FG, its phenology continues in two ways: plants that go through the prematurity stage have only basal leaves, and from mid to late June, their vegetative growth stops, and the leaves begin to dry out. These leaves are easily separated from the roots by the wind. However, the roots remain in the soil and grow again the following year. In plants that are in the last year of their life, flowering begins from the middle to the end of May. The sowing date is from the end of June to the middle of July and the ripening of the seeds happens at the end of July. November and December are the best times to plant FG seeds. The seeds of this plant begin to germinate and grow at 3 to 5 °C. In order to break the dormancy period of the seed and its stratification, it needs to pass a cold period between 3 to −15 °C for 15 to 45 days.

FG shows important applications in cosmetics, pharmaceuticals and animal breeding [6]. In particular, the cosmetic industry requires increasingly greater quantities of FG for its perfume [7]. Indeed, the resin is used for incense, and, above all, as a base for many known fragrances [8]. In the pharmaceutical field, FG-based products are considered energizers, mucolytics and pain relievers for the stomach and joints. The resin of FG is used as a cosmetic in skin care creams. In addition, other authors report an anti-parasitic effect for humans and farmed animals [6]. Finally, in the zootechnical field, some varieties of FG are dried and used to enrich the food of farm animals with nutrients. Some anecdotal observations on livestock report warming effects and an increase in fertility [9]. Like other plant species that are exploited for their therapeutic potential [10,11,12,13,14], FG is among the main plants exploited for its resin [6,15].

Environmental factors such as climate features, topography conditions and soil characteristics affect the establishment of habitats in any region considerably [16]. The distribution of plant species in rangeland ecosystems is not accidental; rather, environmental factors such as climate, soil, topography and human activities play an important role in the expansion of plants [17,18]. Some authors have shown that the establishment of plant communities in mountainous areas is mainly affected by climate factors, and in low-lying areas and rolling hills by soil factors [19,20,21,22,23]. Therefore, it seems that regarding the establishment of FG in the highlands, climatic factors have the greatest role in the distribution and establishment of this plant. This plant is highly resistant to severe cold and frost in mainly semi-arid areas, and it usually grows well in cold and ultra-cold Mediterranean regions with an average annual temperature between 3.5 and 12 °C, the minimum absolute temperature being less than −30 °C and the maximum absolute temperature 40 °C. Areas with an average annual rainfall of 300–450 mm, in which most of the precipitation is snow, are suitable for this plant. Shallow soils, sometimes semi-deep, medium to heavy texture (loam, loamy sand, loamy clay and mostly clay loam), calcareous, sometimes up to about 30% lime and without salinity and alkalinity, are desirable for this plant [24].

Despite these considerable applications, even today it is difficult to cultivate FG due to its particular conditions of growth and development [25]. Furthermore, the lesions induced on the surface of the stem of FG to produce the resin are deep and often lead to the death of the plant [26]. Therefore, the growing demand of the cosmetic and pharmaceutical industry for these species and the alterations of natural habitats, as reported by many authors [6], could lead to its extinction in the wild.

In this manuscript, various ecological analyses are reported on some areas of spread of FG in Iran in order to identify the physical, chemical and biological parameters of four defined areas where the spread of FG seems to be most in crisis. In this way, the natural resources department of the government could plan a long-term strategy to decline the amendment that would likely lead to extinction.

2. Materials and Methods

The main objective of this work was to identify the factors affecting the distribution of FG. For this reason, initially, a review of the scientific literature on FG habitats was performed. Next, climatic information as well as other characteristics were analyzed in a GIS environment (Figure 1). All the meteorological data were provided by the Zanjan Province meteorological organization from 1955 to 2014 initially. To investigate the anthropic effect on the distribution and biodiversity of FG in northwest Iran, four main habitats were selected, and edaphic, climatic and ecological parameters were recorded. In particular, four natural FG habitats were subsequently identified, as shown in Figure 2. According to the FG distribution, the representative area was identified inside each natural habitat, and three points were randomly selected in each area. Then, the information from nearby meteorological stations was collected. In particular, data relating to average temperatures and rainfall (monthly and yearly) from 1955 to 2014 were collected and processed.

In the next step, the ecological traits of FG were recorded from habitats selected (

Table 1. Estimation of climatic parameters by location altitude.

Climate Parameter	Aghzavaj	Kaleh-Sar	Shilander	Taham	Used Formula
Precipitation	408	423	408	415	Pre = 0.116 Alt + 125.25
Average Temperature	8/6	8	8/4	8/3	Tmean = 20.816 − 0.005 Alt

). To do this, three linear transects of 150 m were placed in each habitat and 10 plots (2 m²) on each transect were sampled and studied. In each plot, coverage and density of FG and associated species were measured and recorded.

Soil sampling was performed along each transect at three points (beginning, middle and end of the transect) by digging profiles to the depth of rooting. Soil properties, such as texture by the hydrometer method [27], salinity by the saturated mud extract method [28], acidity by the saturation mud method using pH meter [29], organic carbon by the Walkley Black method [30], phosphorus content by the colorimetric method [31], nitrogen content by the Kjeldahl method [32], potassium content by flame photometer [33] and the amount of neutralizing materials by the reverse titration method [34], were determined in the laboratory. In addition, elevation was determined using an altimeter, geographical directions were determined using a compass and slope percentage was determined using a slope gauge for each habitat to estimate the climatic parameters (Table 1).

The project database was prepared with collected information about climate, the soil of specific habitats and topographic conditions. Climatic parameters such as precipitation, average and absolute minimum and maximum temperature were predicted using the Inverse Distance Weighted (IDW) interpolation method by prebuilt procedures in the ArcGIS software. IDW is an easy technique, which uses linear combinations of weights at known points to estimate unknown location values. In interpolation models, Z(s_o) equals the values at unknown locations and is determined by the weighting value (λ_i) and values at known locations Z(s_i).

$$\begin{gathered} \mathrm{Z}\left({\mathrm{s}}_{\mathrm{o}}\right)={\displaystyle \sum }_{\mathrm{i}=1}^{\mathrm{n}}{\mathsf{\lambda }}_{\mathrm{i}}\mathrm{Z}\left({\mathrm{s}}_{\mathrm{i}}\right) \\ {\mathsf{\lambda }}_{\mathrm{i}}=\frac{{\left[\mathrm{d}\left({\mathrm{s}}_{\mathrm{i}},{\mathrm{s}}_{\mathrm{o}}\right)\right]}^{\mathrm{p}}}{{{\displaystyle \sum }}_{\mathrm{i}=1}^{\mathrm{n}}{\left[\mathrm{d}\left({\mathrm{s}}_{\mathrm{i}},{\mathrm{s}}_{\mathrm{o}}\right)\right]}^{\mathrm{p}}} \end{gathered}$$

In the IDW equation, d(s_i,s_o) is the Euclidean distance between s_i and s_o. P is a power value that controls how fast the weights tend to zero as the distance from the location increases. The higher the exponent, the more influence nearby data will have on the predicted values [35]. After basic layers preparation, other auxiliary layers such as slope layer, slope direction and topographic elevation were prepared using ArcGIS procedures with scale 1:25,000 and fabrication of TIN and DEM models. Then, the factors affecting FG distribution in the rangelands were combined. Therefore, homogeneous and similar areas of natural habitats were extracted, and thus an FG distribution map of the Zanjan Province was obtained and validated with existing documents. Finally, the obtained data was analysed, and the reasons for FG distribution reduction in the natural habitats of the Zanjan Province were concluded.

3. Results and Discussion

Collected data analysis revealed that the main factors affecting FG diversity include misuse of FG-distributed areas for forage cultivation, grazing livestock and improper harvest by local farmers. Meanwhile, pests have been observed on FG stems from Curculionidae species, damaging the stem and leading to lower seed production.

3.1. The Main Habitats of FG Characteristics in the Zanjan Province

The results show that FG constituted more than about 15% of the total abundance of species present in the habitats considered. Furthermore, given the ecological diversity of the habitats studied, these data highlight the ability of FG to distribute itself in multiple ecosystems compared to the other considered species (

Table 2. Characteristics and vegetation status of FG habitats in the studied areas.

Plant Species	Elevation	Density	Stone and Gravel	Bare Soil	Litter	Vegetation Cover
	m	Plant/ha	%				Habitat
- Ferula gummosa Boiss., 15.6%	2430	12,000	43	13	3	41	Aghzavaj
- Pimpinella tragium Vill., 8%
- Silene bupleuroides L., 9%
- Thymus kotschyanus Boiss. & Hohen., 10.7%
- Others, 56.7%
- Ferula gummosa Boiss., 15%	2530	16,800	32	14	3	51	Shilander
- Festuca ovina L., 7%
- Onobrychis cornuta (L.) Desv., 9%
- Silene bupleuroides L., 9%
- Tanacetum polycephalum Sch. Bip., 9%
- Others, 51%
- Ferula gummosa Boiss., 18%	2577	17,200	35	16	4	45	Kalasar
- Alopecurus textilis Boiss., 8%
- Centaurea aucheri (DC.) Wagenitz, 6%
- Prangos ferulacea (L.) Lindl., 6%
- Thymus kotschynus Boiss. & Hohen., 8%
- Others, 54%
- Ferula gummosa Boiss., 16%	2490	8800	32	10	3	55	Taham
- Acantholimon festucaceum (Jaub. & Spach) Boiss., 12%
- Elymus transhyrcanus (Nevski) Tzvelev, 16%
- Onobrychis cornuta (L.) Desv., 16%
- Silene bupleuroides L., 9%
- Others, 31%

). Furthermore, given the distribution of FG, its exploitation would lead to a strong decrease in biodiversity in the areas considered. Likewise, it is observed that the amount of stone and gravel in the studied habitats is significant, and it seems that this factor is effective in the early stages of growth and establishment of the FG. Considering the range of species distribution in the studied habitats, it is observed that the elevation factor is one of the most influential factors in the distribution of FG. In this regard, Egyptian researchers have also considered the various environmental factors on plant communities as a crucial element and have described the characteristics of elevation, slope and direction as the most important factors [36]. On the other hand, it seems that the destruction of these habitats for many years due to improper and unscrupulous human exploitation has forced FG to take refuge in mountainous areas with scattered rocks to allow its growth and survival.

3.2. Climatic Characteristics of the Studied Areas

3.2.1. Total Annual Rainfall and Average Temperature

We referred to the rainfall and annual temperature data of synoptic stations adjacent to the study area, in order to obtain the amount of rainfall and temperature in the region. The results are presented in Figure 3.

According to the calculations, rainfall and the average temperature of all habitat areas were in the range of 423–408 mm and 7.8–8.8 °C, respectively, so that both parameters were among the ideal characteristics for the growth of FG [24].

In order to evaluate the water required by the plant in the different phenological stages, the monthly distribution of rainfall was considered (Figure 4). Figure 5 shows the monthly distribution pattern of the necessary rainfall in the different stages of germination, vegetative growth and reproductive growth of FG.

Several studies have shown that the FG plant is highly resistant to cold and frost, and grows mainly in semi-arid and sometimes cold and ultra-cold Mediterranean regions, with an average annual temperature between 3.5 and 12 °C [37,38,39]. This plant grows well at an absolute minimum temperature below −30 and absolute maximum temperature below 40 °C [40]. Our study showed that the absolute minimum temperature of FG vegetative growth period (from the second half of March to July) is equal to −15 °C and the absolute maximum temperature in the hottest month of the year (July) is equal to 34.5 °C. Therefore, these environmental factors cannot be a limiting factor for the distribution and establishment of FG in the region.

3.2.2. Topography

Topography is one of the factors affecting the growth and distribution of plants. Important and effective topographic parameters include habitat height, type of elevation (plains, foothills, rolling hills and mountains), amount and direction of the slope. Accordingly, the slope is mainly north and northeast with a slope of 55 to 70 degrees, and an elevation range above 2200 m is suitable for the growth of FG in the Zanjan Province (

Table 3. Sampling sites characteristics in the main habitats of FG in Zanjan Province.

Geographical Direction	Height	Percentage Slope	Latitude	Longitude	Area Name
	(Meters above Sea Level)
N	2511	60	365,001	483,750	Shilander
NE	2577	70	370,209	482,818.5	Kalesar
NE	2430	55	363,451.2	485,442.2	Aghzavaj
NW	2490	65	365,011.6	483,735.9	Taham

).

3.2.3. Soil

The results show that in the habitats where FG grows, the soil was mostly shallow, sometimes semi-deep and consisting mainly of loam, loamy sand, loamy clay and mostly clay loam. Climatic factors, along with soil properties, change the vegetation by determining soil moisture (Noy-Meir, 1973). As indicated in

Table 4. Soil characteristics of four FG natural habitats in the Zanjan Province.

	Ec	pH	TNV %	Oc %	K (ppm)	P (ppm)	N %	Sand %	Silt %	Clay %
Aghzavaj	0.46	6.9	1	2.68	6.26	9.26	0.26	56.0	35.6	8.3
Shilander	0.69	7.8	3	1.46	245.6	11.7	0.14	41.3	44.0	14.6
Kalasar	0.63	6.9	2.13	2.14	219.3	6.33	0.12	56.6	33.6	10.6
Taham	0.29	7.3	4.7	2.47	384.6	12.5	0.14	31.3	54.0	18.0

, soil salinity was very low (less than 0.7 dS/m) and soil acidity was in the neutral range (6.9 to 7.33). Soil organic carbon was relatively high, but the amount of nutrients such as phosphorus and potassium was less than optimal in these soils. The results of soil samples analysis of the natural habitats of FG in the Zanjan Province are presented in Table 4.

Soil texture characteristics (amount of clay, sand and silt) and elements concentration in the soil (amount of potassium and nitrogen) are important and influential factors on FG distribution as observed by other authors [22,24,26]. The structure of the soil with its vegetation influences the amount of humidity and plant elements available, the water retention capacity and permeability of the soil, the organic matter present, the nutrient cycle of the soil and the depth of rooting of the plants.

3.2.4. Combined Data Analysis

In order to define the climatic, topographical, demographic and pedological areas of the natural habitats of FG studied through the Geographic Information System, a map of these habitats was drawn up with the ArcGIS software (Figure 5). This map shows homogeneous areas with the ability to support the establishment of FG. Several factors have been identified as main elements making changes in vegetation in FG habitats. These elements include land use conversion, harvesting fodder, grazing livestock, improper operation, pests and diseases of FG in the region.

3.3. Factors Affecting Vegetation Change

3.3.1. Land Use Conversion

The increasing rate of rangeland plants’ population growth, followed by the increasing human need for food, have led farmers in different countries to exploit poor land with high erosion and low production potential [41,42]. Changes in land management and use, as well as tillage functions, have an abundant impact on organic matter and their physical, chemical and biological properties [42,43]. Reduction in organic matter due to the lands’ management change has been reported by researchers [44,45]. In other words, tillage operations erode the soil, severely degrading it and greatly reducing its fertility. The conversion of land use to drylands was observed several times during the field visits to the habitats of FG. Figure 6A is an example of land turned into Medicago sativa L. in the Shilander area.

3.3.2. Harvesting Fodder and Grazing Livestock

Based on the available documents and reports, the condition of most rangelands is poor or very poor, and the percentage of undesirable species is very high compared to desirable rangeland species in Iran [18]. This condition can lead to a decrease in grazing production per unit area. Indeed, due to the lack of good forage, livestock is forced to feed on poor species from a nutritional point of view. For this reason, breeders are forced to enrich the nourishment of livestock with other plant species that grow in the areas intended for grazing. As previously mentioned, FG is a source of forage, especially during the winter (Figure 6B). Jamsranjav and colleagues argued that as long as the livestock population is in equilibrium with the ecosystem, precious resources such as water, soil and plants will not be harmed [46]. Therefore, proper use of land for grazing will lead to preserving the plant species of the habitat. It follows that in itself, the use of land for grazing does not damage the ecosystems where FG develops. Unfortunately, field observations of the areas studied showed that FG is being collected indiscriminately and intensively together with other species to provide winter forage. Undoubtedly, this type of exploitation can be considered a serious problem for the growth, development, diffusion and reproduction of FG in the coming years.

3.3.3. Improper Operation

Individuals’ improper exploitation methods have resulted in the destruction of a large part of the natural habitats of Ferula species in Iran [47]. In the several visits of its natural habitats, FG’s flowering stems were seen to have been completely cut off (Figure 6C,D). In our opinion, if the improper operating process continues in the same way, the regeneration of the FG plant may be difficult after several years. Because of the monocarpic nature of this plant, it blooms once every 8–12 years.

3.3.4. Pests and Diseases of FG in the Region

Based on field evaluations, some Curculionidae species pierce the stem of the FG and lay their eggs inside, where their larvae subsequently grow (Figure 7A,B). However, the larvae rarely settle in the flower stems, as this allows the plant to pass the stages of pollination and seed production before the damage of this parasite spreads. Furthermore, FG is a latex content plant, meaning it responds to wounds, cuts and cracks by secreting latex. The limited number of holes is spawned successfully by female weevils. Most of these holes are filled quickly by latex during drilling due to this inherent property of the FG plant. A species of aphid is the second sub-parasite of FG. These aphids feed on the flower stem of FG. They are protected against their natural enemies (especially ladybugs) by cooperating with some species of ants (Figure 7C,D). However, thanks to the short life of the FG flower stem and the presence of natural enemies of the aphids, the damage of these parasites is almost never lethal for the life of FG.

3.3.5. Proposed Solutions for FG Regeneration in Natural Habitats

The excessive density of livestock and the growth of the human population are at the root of the loss of precious species such as FG and the reduction in biodiversity. The strategies applied to stop this misuse of natural resources and restore the growth and spread of FG include its cultivation and the delimitation of areas intended for grazing [48]. Indeed, limiting grazing to well-defined areas (delimited by fences) allows the restoration of plant species in areas outside the fences. In these areas, the composition of vegetation changes as the duration of grazing restrictions increases [49]. Indeed, in areas excluded from grazing, there is an increase in forage species due to an increase in their ability to reproduce and expand. It follows that the protection of FG can also be implemented with attention to the breeding strategies of grazing livestock.

Cultivation and regeneration of plants in natural habitats is another effective management and conservation measure in degraded pastures. In general, this strategy can be applied to rebalance and restore the habitat of plant species such as FG, and to adopt a correct management of grassland ecosystems. In this strategy, ex situ germination with subsequent reintroductions to the wild, respecting the population’s genetic diversity, would be implemented.

4. Conclusions

The results collected in this study on the ecology of FG have shown how the different ecosystems in which this species lives show physical-chemical characteristics suitable for the growth and spread of FG. At the same time, anthropic activities have a destructive effect on the ecological niches of FG. In particular, the indiscriminate exploitation of land aimed at grazing livestock reduces biodiversity and alters the habitat of FG. Population growth and the consequent increase in the human need for food is considered in many parts of the world to cause the disappearance of many wild plant and animal species [11]. Farmers and ranchers exploit poor and marginal lands, which mainly have a high erosion potential and a low production potential [50]. The soil of these areas has a natural yield and a specific organic matter for the endemic plant populations that live there. The indiscriminate exploitation of these soils reduces biodiversity and disrupts the balance of ecosystems, with a great impact on organic matter and other physical, chemical and biological properties of the land, leading to soil desertification. This anthropic action on the environment has also affected the habitats of the FG. Lack of attention in pruning, indiscriminate use as forage and the disappearance of plant biodiversity could lead to the reduction in and subsequent extinction of FG. This important problem observed for FG can be observed in many other plant species living in other ecological niches.

In conclusion, many plant species are at risk of extinction in the world due to mankind’s improper lifestyle. FG has shown many adaptive capacities to different ecosystems and to attacks by insects. However, the excessive exploitation of the plant and the soil could reduce the spread of FG and lead it to extinction. Only greater awareness and sustainability of human societies towards the environment will be able to preserve biodiversity while avoiding the extinction of many plant species such as FG.