European Journal of Medicinal Plants 4(9): 1087-1097, 2014

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Observations on Flowering and Fruiting in Commiphora wightii (Arnott) Bhandari

Hema Singhal1, Arti Gaur1 and U. K. Tomar1*

1Forest Genetics and Tree Breeding Division, Arid Forest Research Institute, Jodhpur, India.

Authors’ contributions

This work was carried out in collaboration between all authors. Author UKT designed the study, performed the statistical analysis, wrote the protocol, and author HS wrote the first draft of the manuscript. Authors HS and AG managed the field study. All authors read and approved the final manuscript.

Received 21st March 2014 st Original Research Article Accepted 21 May 2014 Published 13th June 2014

ABSTRACT

The present work aims to document the phenological diversity of flowering and fruiting in guggul with reference to climate. Commiphora wightii flowering and fruiting patterns were monitored in Kaylana (Jodhpur, Rajasthan) over a period of 24 months. Observations on flowering and fruiting phenology were carried out monthly, from March 2010 to May 2012. Flowering and fruiting patterns were studied qualitatively as well as quantitatively. Flowering and fruiting occurs throughout the year but maximum observed in April and May, respectively and second time in November. Strong positive correlation between flowering/fruiting and monthly mean daily maximum temperature (Flowering r = 0.762, P˂ 0.01, Fruiting r = 0.714, P˂ 0.01) indicate that flowering and fruiting are enhanced by higher temperatures. Fruiting was negatively correlated with mean monthly relative humidity at 6 O’ clock in the morning (r = -0.59, P ˂ 0.05). Regression analysis also revealed positive linear relationship between mean monthly maximum temperature and 2 flowering percentage (R = 0.58118, F1/10 = 13.87652, P ˂ 0.01). Similarly, a positive but 2 quadratic relationship (R = 0.704, Fx/y = 10.71643, P ˂ 0.01) was also observed between flowering and mean monthly minimum temperature.

Keywords: Commiphora wightii; guggul; phenology; flowering; fruiting.

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*Corresponding author: Email: [email protected]; European Journal of Medicinal Plants, 4(9): 1087-1097, 2014

1. INTRODUCTION

Commiphora wightii, locally known as ‘Guggul’ or ‘Guggal’ is an important ancient medicinal plant belonging to the family Burseraceae. It is a small tree, reaching 4 m maximum height. The Sanskrit definition of the term "guggul" is "one that protects against diseases". The extract, called guggulipid comes from the guggul tree and has been used in Ayurvedic medicine, a traditional Hindu medicine, for nearly 3,000 years in India [1]. Guggulsterones which are mentioned in the marketing of guggul products are the extract isolates of ketonic steroid compounds. Based on research, these compounds are considered to be responsible for guggul's cholesterol- and triglyceride-lowering actions. Guggul significantly lowers serum triglycerides and cholesterol as well as LDL and VLDL cholesterols (the "bad" cholesterols) by approximately 25%. At the same time, it raises levels of HDL cholesterol (the "good" cholesterol). Several patents have been assigned for guggul uses in cosmetics [2].

Ruthless exploitation and lack of cultivation practices of this species has led to decline in its population continuously making this plant vulnerable and was categorized as ‘data deficient’ in assemblage of IUCN in 2008. Though, C. wightii is assigned to the DD (Data Deficient) category ver. 2.3 (1994) of the Red Data Book of IUCN, the Government of India has included it under RET (Rare, Endangered, Threatened) category [3]. Being such an important plant it has been selected by Medicinal Plant Broad, New Delhi and providing lot of funds for its conservation and improvement.

In 2008, NMPB (National Medicinal Plant Board, India) launched a mega project in collaboration with CIMAP (Central Institute of Medicinal and Aromatic Plants, Lucknow), CAZRI (Central Arid Zone Research Institute, Jodhpur), AFRI (Arid Forest Research Institute, Jodhpur), DAMPR (Directorate of Medicinal and Aromatic Plants Research, Anand) and Rajasthan & Gujarat SFDs (State Forest Departments) to carry out research on the conservation of genetic resources and development of superior oleo-gum resin of this valuable species [4].

Phenological studies particularly flowering and fruiting are vital to develop viable conservation and breeding strategies and using biotechnological tools for improvement. Such studies also provide knowledge about the pattern of plant growth and development as well as the effects of environment and selective pressures on flowering and fruiting behavior [5]. Guggul plant exists in three forms i.e. male, female and andromonoecious [6]. However, there is very poor information on the flowering and fruiting of this plant. This paper aims at minimizing this gap of information by evaluating C. wightii in terms of its flowering and fruiting phenology. Thus, a study was initiated on guggul to: 1) provide descriptive information on the flowering and fruiting progression for the plants occurring in an area and 2) investigate the relationships between climatic factors and flowering and fruiting patterns.

2. MATERIALS AND METHODS

2.1 Study Site

The present study was carried out at Kumatia enclosure (26°19N, Latitude; 72°57E, Longitude and 274 m altitude) Forest area, which is situated at Kaylana-Jodhpur-Manodre plateau in Jodhpur district of Rajasthan, India. The Kaylana area covers several rugged scattered hills which are mostly made of sandstone, granite and rhyolite. Naturally growing population of Commiphora wightii in 20 ha area at Kaylana was selected for studies. It was a

1088 European Journal of Medicinal Plants, 4(9): 1087-1097, 2014 rocky area which was having Acacia senegal, Acacia nilotica, etc. along with Commiphora wightii plants. The soil is fine, reddish gritty. pH ranged from 7.85 to 9.24 up to 15 cm depth and 8.53 to 8.80 between 15 to 30 cm depth [7].

2.2 Climatic Data

Monthly values for rainfall, minimum and maximum temperatures, wind speed, sunshine and relative humidity at 6 O'clock in the morning (I) and at 6 O'clock in the evening (II) were obtained from CAZRI (Central Arid Zone Research Institute) agricultural meteorological station (Table 1) of Jodhpur. The climate is hot and dry with three distinct seasons. The summer season, from April to June, is extremely hot with temperature soaring to 43.4ºC while May. The rainy season is from July to September with 90% of annual rainfall (458 mm) during this period and the dry cold winter season is from October to February with temperature dropping to 9.1ºC in January. The areal distance from CAZRI to study site is about 7 km. only and climatic variation between the study site and meteorological station was also negligible.

2.3 Data Collection

Ten quadrates (30x30m, 0.09 ha area) were taken randomly from different locations of Kaylana area, which were having a total of 66 plants. All the plants were tagged and just to see the age effect on flowering and fruiting girth of all these plants were also recorded at 5 cm above the ground. Girth of these plants ranged from 12 to 75 cm. All the plants were female. Flowering and fruiting data for all the plants were recorded on monthly basis from March 2010 to May 2012. While monitoring, each plant containing flowers and fruits was noted.

The survey involved qualitative and quantitative data collection from marked individuals. We characterized the flowering/fruiting behavior of a plant by two variables: percentage of plants in flowering/fruiting stage and the intensity of flowering/fruiting (flowers/fruits per plant on relative score basis). In order to measure the flowering and fruiting intensity for each individual/population, following method/formula was adopted to rank them between 0 to 10 numbers. A branch was considered in flowering/fruiting only when it is having at least one open flower/one fruit on it.

1. Flowering/fruiting intensity of individual plant i ,

2. Flowering/fruiting intensity of population under= study× 10I ∑ = ∑ × 10 Where, n is the number of branches in flowering/fruiting and N is the total number of branches in a plant.

Female flowers were very small, 3-4 mm long and their growth and development is asynchronous even in same branch of a plant. On the same branch closed flowers (Fig. 1A), opened flowers (Fig. 1B) and both closed and open flower (Fig. 1C) were observed. Similarly, maturity levels were also varied in the fruits growing on a plant (Fig. D & E). At population level, for each monitoring year, peak flowering and fruiting refer to the months in which the number of individuals observed in that phenophase reached a maximum.

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Fig. 1. Closed Flowers (A), Open flowers (B), Closed and open flower on same location on a branch (C), Immature fruits (D) and Mature fruit (E)

2.4 Statistical Analysis

The relationship in flowering and fruiting between monitoring seasons was expressed in terms of the percentage of individuals with identical phenological expression. Pearson’s correlation coefficients were used to test the relationship between phenological events (flowering and fruiting) and the climatic variables assessed. Correlations between the monthly percentage of individuals in flowering/fruiting and monthly rainfall totals, monthly means of daily maximum and daily minimum temperatures, relative humidity, wind speed and sunshine were examined.

3. RESULTS

3.1 Flowering/Fruiting Frequency

The monthly flowering data of total 66 plants indicate that there were always some plants in flowering stage throughout the year. But the percentage of flowering plants was bimodal with two peaks. The major flowering period of this plant is from April to July, where more than 90% plants (April, May & June all 66 and in July 60 plants) were in flowering stage. Second

1090 European Journal of Medicinal Plants, 4(9): 1087-1097, 2014 flowering phase reaches a small height in November, where about 40% (27 out of 66) of plants bear flowers. Almost similar pattern was recorded for fruiting with very little lower percentage (Fig. 2).

Fig. 2. Flowering and fruiting behavior of Guggul plants recorded in the year 2010-11

3.2 Flowering/Fruiting Intensity

Data was also collected on flowering and fruiting intensities by using relative scores as mentioned in material and methods. Highest intensity of flowering was found in April, where average relative score is about 7.8, whereas fruiting intensity was highest after one month (May) at an average relative score 7.5. Second small peak was recorded in November for both flowering and fruiting intensities (Fig. 3). It is worth to mention that some flowers and fruits were present even in the adverse periods for flowering/fruiting.

3.3 Effect of Girth Class

All 66 plants were clustered in four groups on the basis of girth viz. 12-30 cm, 31-40 cm, 41- 50 cm and 51-75 cm. One way ANOVA analysis revealed insignificant differences in flowering/fruiting percentages and intensities due to differences in girth.

3.4 Climatic Effect

Phenology of Commiphora wightii was strongly seasonal. Two parameters recorded on flowering and fruiting exhibit annual synchronization with mean maximum temperature and sunshine hours with two peaks. It is also clear that higher mean maximum temperature (>35ºC) and sunshine (>9.5 hrs) enhanced flowering and subsequently fruiting significantly

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(Table 1). Lowest flowering and fruiting was recorded in February (7.6 & 6.0%) and September (10.6 & 3.0%). Probable reason for the low value in these two months may be adverse effect of high rainfall on flowering and fruiting and diverting resources to vegetative growth.

Fig. 3. Flowering and fruiting intensity in Guggul plants recorded in the year 2011-12

Table 1. Climatic variations in Jodhpur (March 2010 to February 2011)

Month Temperature Relative Rainfall Wind Sun Monthly Monthly (ºC) Humidity (mm.) speed shine Flowerin Fruiting Max. Min. I II (km/hr.) (Hrs.) g % % January 24.5 9.1 69 20 0.0 2.8 8.6 12.1 9.1 February 27.5 13.6 70 29 14.8 3.5 8.8 7.6 6.0 March 37.2 20.5 41 13 0.0 4.0 9.9 28.8 51.5 April 41.3 26.4 35 12 0.2 5.9 9.4 100.0 92.4 May 43.4 29.5 40 13 0.0 8.3 9.0 100.0 95.5 June 40.0 28.9 57 29 45.4 8.7 9.1 100.0 97.0 July 37.2 27.8 77 49 133.9 6.5 6.0 90.9 97.0 August 33.6 26.4 87 63 120.7 4.0 5.6 30.3 21.2 September 33.8 23.7 81 53 202.9 2.8 7.3 10.6 3.0 October 36.5 21.0 61 25 0.0 2.2 9.5 25.8 18.2 November 29.1 17.5 73 41 39.8 2.6 6.2 40.9 33.3 December 25.1 9.9 73 28 17.3 2.3 7.9 30.3 21.2

However, Pearson’s correlation (Table 2) between numbers of individuals in flower/fruit each month (all plots combined) and relative humidity I, mean monthly rainfall, wind velocity and sunshine not showed any significant correlation. There was a strong positive correlation between flowering and monthly mean daily maximum temperature (r = 0.762, P < 0.01) and

1092 European Journal of Medicinal Plants, 4(9): 1087-1097, 2014 also between fruiting and monthly mean daily maximum temperature (r = 0.785, P < 0.01) showing that flowering/fruiting occurred more often in hotter months. Flowering (r = 0.723, P < 0.01) and fruiting (r = 0.714, P < 0.01) were also positively correlated with monthly mean daily minimum temperature. Fruiting was inversely related to mean monthly relative humidity (r = −0.590, P < 0.05) at 6 O'clock in the morning.

Table 2. Pearson Correlation (r) of percent flowering and fruiting in C. wightii and climatic variations at Kaylana, Jodhpur site

Temp. Temp. R.H. (%) R.H. (%) Rainfall Wind Sunshine max. min. I II mean velocity monthly Flowering 0.76** 0.72** NS NS NS NS NS Fruiting 0.78** 0.71** -0.59* NS NS NS NS Temp. = temperature; max. = maximum; min. = minimum; R.H. = relative humidity ** Correlation is significant at p<0.01, *Correlation is significant at p<0.05 and NS – Non significant at p<0.05

Regression analysis between monthly data on flowering percentage and mean monthly maximum temperature revealed highly significant positive linear relationship (R2 = 0.58118, 2 F1/10 = 13.87652, P<0.01) as shown in (Fig. 4). Similarly, a significant positive quadratic (R = 0.70427, Fx/y = 10.71643, P<0.01) relationship between flowering percentage and mean monthly minimum temperature (Fig. 5) was also observed. Conclusively, high flowering and fruiting percentage (above 90%) was recorded when mean monthly minimum temperature and mean monthly maximum temperature was between 26.4 and 37.2ºC, respectively.

Fig. 4. Scattergram plot of the Mean Monthly Maximum Temperature (ºC) and Flowering (%) and the regression model best fit straight-line describing the linear relationship between the two variables

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Fig. 5. Scattergram plot of the Mean Monthly Minimum Temperature (ºC) and Flowering (%) and the regression model best fit curve-line describing the quadratic relationship between the two variables

4. DISCUSSION

Guggul flowering pattern is periodic, extended and asynchronous and fruiting pattern is periodic, extended and fruit maturation is lengthy, which was equal to or more than 4 months [8]. They also reported the flower initiation in guggul in April. Orwa et al. [9] reported unimodal flowering (October to December) and fruiting (October to January) and Tandon et al. [10] reported two flowering peaks in guggul i.e. April/May and October/November in guggul but both papers do not provide site details and flowering and fruiting data. Thus, detailed studies on annual flowering and fruiting patterns are scanty in this important as well as threatened medicinal plant.

Present studies provide some more detailed and useful information on annual flowering and fruiting patterns and climatic influence on these events. The flowering and fruiting of plants is known to be controlled by a number of environmental factors such as temperature, light, rainfall, relative humidity etc. Plants have developed their genetic makeup to adjust in these conditions. On flowering span basis, they are separated into long flowering duration (Gaillardia grandiflora, Salvia spledens, Zinnia elegans, etc.) and short flowering duration plants (Centranthus ruber, Linaria maroccana, Pentas lanceolata, Terminalia mucronata, etc.). C. wightii comes in the class of long flowering and fruiting duration plants as also observed in present studies.

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We observed a bimodal flowering and fruiting pattern in C. wightii in Jodhpur climatic conditions. Bimodal flowering pattern has also been observed in some other species like Metadina trichotoma, Liothocarpus sootepensis [11], Ferocactus cylindraceus [12] and Azadirachta indica [13]. Bimodal flowering phenologies have been recorded in a Bolivian dry forest [14] and in a tropical lowland forest [15]. The bimodal phenological patterns at different habitats may be attributed to different biotic and abiotic factors. According to McIntosh ME [12] the most likely explanation is that it is an adaptive response to the abundant summer rains.

Climatic annual patterns play vital role in inducing flowering and fruiting twice a year. In Jodhpur conditions, sunshine is also exhibiting two peaks, one broad peak and another small and narrow peak which are similar to flowering and fruiting patterns. The sunshine determines the temperature regime that influences the flowering pattern and thus, follows the same bimodal pattern. Both flowering and fruiting happened during sunniest periods, as a possible causal effect of photosynthesis rate augmentation. The use of available energy to grow flowers and fruits without storage in specialized tissues is thereby optimized [16]. This result is consistent with most of the phenological studies in sclerophyllous vegetation stands that showed more than half of flowering peaks occurred during the sunniest months [17].

Flowering in guggul tends to be concentrated in the months when a combination of climatic factors ensures dry conditions and the atmospheric relative humidity has been low. Janzen [18] attributed flowering in the dry season to the necessity for avoiding competition for physiologically active sites within the individual and to the availability of pollinators. The association of intensified flowering activity with hot dry weather is a commonly reported phenomenon in tropical forests. The most likely factor that triggers flowering during the dry season is water stress [19] but high temperatures, hours of sunshine, or internal biological clocks may also play a role. One possible advantage to flowering during the dry season is that because many trees are leafless at this time, flowers are more visible and accessible to pollinators.

Thus, temperature and radiation duration are assumed to be the climatic parameters that have the greatest influence on guggul phenology. When moving away from the equator, phenological patterns should be more influenced by daylength and temperature (which became more variable) and less by rainfall [20]. Daylength and solar elevation (latitude) determine the light and temperature regimes that influence plant primary production [17,21].

There is great scope of selecting different genotypes having different genetic potential of flowering and fruiting patterns due to asynchronous flowering/fruiting as well as long period of flowering and fruiting. Our preliminary studies also indicate differences in flowering/fruiting period and intensity amongst these 66 plants at common site in Jodhpur. Phenological data from other populations growing in different agroclimatic zones are needed to develop a dynamic model of phenological expression and its interaction with environmental variables.

5. CONCLUSION

Guggul plant bore flowers/fruits throughout the year. However, the percentage of plants in flowering and fruiting as well as the intensity of flowering and fruiting depict two unequal peaks in Jodhpur conditions. Amongst various climatic factors under this study, mean motherly temperature has major role to regulate annual flowering and fruiting percentage. Annual pattern of flowering and fruiting plants percentage was very much similar to mean monthly maximum temperature pattern.

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Correlation and regression methods established linear relationship between flowering percentage and mean monthly maximum temperature. Whereas, flowering plant's percentage relationship was quadratic with mean monthly minimum temperature.

CONSENT

Not applicable.

ETHICAL APPROVAL

Not applicable.

ACKNOWLEDGEMENT

The authors are thankful to the Authorities of State Forest Department (SFD) Rajasthan for financial support and access to Guggul area at Kaylana used in present study. We are also grateful to AFRI authorities and Mr Thanaram Rathod (RAI) for their support and cooperation in research and office work. Hema Singhal and Arti Gaur acknowledge the award of a Senior Research Fellowship by the CSIR and UGC, New Delhi, India respectively.

COMPETING INTERESTS

Authors have declared that no competing interests exist.

REFERENCES

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Peer-review history: The peer review history for this paper can be accessed here: http://www.sciencedomain.org/review-history.php?iid=556&id=13&aid=4903

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