Research Article | Volume 11, Issue 4, July, 2023

Timing of phenological events and fruit ripening in Ficus palmata forssk. In the Mid Himalayan Region

Jyotsna Tamta Ashish Tewari Krishna Kumar Tamta Shruti Shah   

Open Access   

Published:  Jun 04, 2023

DOI: 10.7324/JABB.2023.113040
Abstract

Ficus palmata Forssk. is commonly growing wild in the Himalayan region of the family Moraceae. A study was undertaken at the Kumaun Himalaya region to evaluate the regeneration, phenology, maturity indices, and nutrition status of F. palmata. The density of F. palmata across the sites ranged between 22 and 122 ind/ha. Seedlings were completely absent in all the study sites. However, saplings were present in low numbers. The seeds were minute, and germination was high ranging between 84.68 ± 2.42 and 95.33 ± 1.64% while the seed moisture content was between 36.33 ± 0.88 and 42.33 ± 0.88% across all the sites. Flowering and fruiting occurred twice a year from March-May to October-December. Only the seeds produced during summer season (April–May) were viable. It is facing high anthropogenic pressure and poor regeneration. There is an urgent need for conservation and large-scale plantation programs. Assessment of the exact time of fruit/seed maturation using physical indicators can help collect viable seeds for regeneration and multiplication of the species. The study could highlight that this species is facing severe regeneration problems. Fruit/seed maturation can disturb its synchronization with the monsoon rains when maximum germination occurs. The study developed baseline data on phenological events for future referencing on the impact of climate change on this species.


Keyword:     Moraceae Phenology Maturity Moisture content


Citation:

Tamta J, Tewari A, Tamta KK, Shah S. Timing of phenological events and fruit ripening in Ficus palmata forssk. In the Mid Himalayan Region. J App Biol Biotech. 2023;11(4):109-118. https://doi.org/10.7324/JABB.2023.113040

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

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1. INTRODUCTION

The genus Ficus universally known as fig, belongs to the family Moraceae [1] and is one of the largest plant genera, with more than 750 species distributed worldwide [2-4]. In India, 115 species of Ficus are distributed throughout the country, and the maximum diversity of the species lies in the North-East region [5]. Ficus species have a diversity of habitations; few are hemi epiphytes, large woody climbers, and trees and shrubs. Most of the Ficus species are good fodder sources. A large number of vertebrates depend for food on Ficus species [6].

Ficus palmata Forssk. is a multiuse tree that belongs to Moraceae family, found growing wild in the Himalayan region, native of North-Western India and Rajasthan regions, Garhwal and Kumaun region, Uttarakhand, Nepal up to 1550 m above the sea level. F. palmata occasionally occurs in the forest but grows well around the villages, fields, and wastelands. F. palmata is a deciduous tree with minor unisexual flowers and deep violet to black fruit inside which numerous, round, and very small seeds are found. The whole fruit and the seeds can be eaten either in the immature stage by cooking as a vegetable or after maturing as fruit. It is one of the top edible wild fruits with medicinal and nutritional properties [7,8].

Several studies show the importance of F. palmata in treating several diseases [9] but very few on its regeneration status, phenological events, fruit/seed maturity, and germination. Shifting in the timing of fruit seed maturation time can severely impact the regeneration of this species. There appear to be no baseline data to compare the changes in the timing of phenological events of this important species coupled with regeneration information.

Ficus species are wild edible species, and the dependency for food on different species of Ficus is very high. In the Himalayan mountains, regeneration of the fodder/edible fruit species is a significant problem. Regeneration of the species, survival, and growth of seedlings depend upon human disturbance, trampling by cattle, and cattle browsing [10]. The successful regeneration of forest species is characterized by a sufficient population of saplings, seedlings, and adults [11].

We studied the regeneration status of fruit/seed-related traits, the timing of fruit/seed maturation, and germination, which is critically needed to develop baseline data to fully comprehend the impact of climate change on this struggling species. (1) In view of the importance of this species-poor regeneration and scanty information on seed/fruit maturity indices, the present study was planned to document the most suitable time for fruit/seed collection and determines the effect of different collection dates on fruit/seed characters and germination essential for its multiplication. (2) Timing of major phenological events was carried out to determine the impact of climatic change compared to previous studies. (3) Nutrient analysis of leaves and fruits was done to determine the suitability of the leaves/fruits of the species as fodder so that large-scale plantations of the species can be undertaken to meet the needs of green fodder during the lean summer months in the hill areas.


2. MATERIALS AND METHODS

2.1. Study Site

The study areas are located between 29’ 22” N latitude and 79’ 38” E longitude. The research was carried out over 2 years (2017 and 2018). Three sites (S1, S2 and S3) were selected between 1136 m~1704 msl. altitude on northeast and northwest aspect [Table 1]. The associated species were Ficus nemoralis Vern., Quercus leucotrichophora A. Camus, Ficus roxburghii Wall., Grewia optiva Drumm., Pinus roxburghii Sarg., Aesculus indica Wall., Cupressus torulosa D. Don ex Lamb., Prunus cerasoides D. Don., Pyrus pashia Buch. and Cedrus deodara Rox. were found as main associates. The texture of the soil was sandy clay loam across all the three sites. The climate of the study sites is subtropical monsoon with high temperatures towards lower elevation and lower temperatures towards high elevation. Rainfall is governed by the southwest monsoon; annual rainfall was 1337.50~1536.40 mm (approx.) during the study period, of which 90% occurred from mid-June to mid-September. In both years, May was the warmest month of the year and December the coldest month, with temperatures ranging from 2.89°C to 25.9°C (Source: S. M. R. A. G. I. C. Tallital, Nainital).

Table 1: Details of selected sites of Ficus palmata.

S. No.Site nameAspectElevation (msl.)CoordinatesDensity (ind/ha)
1Site1 (bhumiyadhar) (nainital district)North west1704N 30°29’70” E 79°13’15”66
2Site 2 (gethiya) (nainital district)North east1136N 29°22’10” E 79°30’28”78
3Site 3 (katyari) (almora district)North east1530N 29°35’29” E 79°38’30”122

2.2. Regeneration Status

For calculating the regeneration of the species 10 quadrats each of 10 × 10 m were placed across all the sites [12]. Density of trees, saplings, and seedlings was estimated following [13].

2.3. Phenology

The phenophases were observed from bud formation to fruit/seed formation. During the field visit, the phenophases were recorded for selected species. To record observation of different phenological events, 05 superior individuals were marked and frequent field visits were made [14]. Phenological records were collected from the last week of March 2017 to the 2nd week of January 2018.

2.4. Maturity Indices

The species produced flowers/fruits twice in the year, Mar-May and Oct-Dec. However, only the data for the period between March and May has been presented. As the fruits from October to December produced non-viable seeds which failed to germinate. Fruit collection was started from the 2nd week of April up to the availability of fruits from marked trees for all three sites at week intervals. Fruits were collected at 1-week intervals directly from the selected trees. Fruits from all trees were combined at one collection date to create a composite sample. Fruits were manually de-pulped to extract seeds. Three replicates of 25 fruits/seeds were taken from the composite sample to determine the different morphological characters of fruits/seeds (size, color, and fresh weight). Fruit and seed weight (100 fruits/seeds) was measured by electronic balance (Model No. PGB 301 accuracy + 0.001 mg Wensar), and fruit and seed size (25 fruits/seeds) were expressed in mm² (length and width) was estimated using (Model No. CD-6” accuracy + 0.02 mm Mitutoyo Co.) digital Vernier caliper. Moisture content% was estimated based on three replicates of fruits and seeds (25) each and assessed on a fresh weight basis by drying at 103 ± 2°C for 16 ± 1 h and then the samples were reweighted according to [15,16]. For germination four replicates of hundred seeds were kept at the top of germination paper in petri-dishes at room temperature. The appearance of the first radicle germination was considered to have started and was studied for 40 days, following [17], the seed germination% was calculated.

The data were analyzed using analysis of variance [18].

2.5. Viability

For viability retention seeds of F. palmata collected at maturity were stored under two conditions in airtight plastic containers placed at room temperature (during day18–26°C and night 3–13°C) and refrigerator (1 and 3°C) [1]. The viability was checked by germinating 3 replicates of 100 seeds every 30 days up to the time seeds germinated (in both year-1 and year-2) [19].

2.6. Nutritive Value

The protein content of leaf/fruit was determined with the help of [20]. Ash was prepared at 550°C in a muffle furnace. Calcium was determined by the volumetric method. Phosphorous was determined by the molybdenum blue method [21,22].


3. RESULTS

3.1. Regeneration Status

The tree density of F. palmata ranged between 22 and 122 ind/ha across all the studied sites. Seedlings were completely absent in all the study sites. Saplings were present in all selected sites except site 1 but the density was low. The total tree density of the site varied between 297 and 554 ind/ha with 1.91 and 26.2 m2/ha−1 TBA across all the sites.

3.2. Phenology

The leaf initiation in F. palmata started in the 3rd week of March and was complete by the 3rd week of April. Flowering and fruiting occurred 2 times a year 1st-time, fruits were visible between the 3rd week of March and the 3rd week of May, and a 2nd time between the 3rd week of October and the 2nd week of December. Seed dispersal also occurred 2 times in a year, and the period of seed dispersal in both seasons was short. The leaf fall started in the 1st week of December and was completed by the 1st week of January [Figure 1].

Figure 1: Phenological events of Ficus palmata (I-IV) weeks of each month I= week 1, II week 2, III = week 3, IV = week 4. L= Leafing; FL = Flowering; FR= Fruiting; SD= Seed dispersal; LF= Leaf fall.



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Figure 2: (a) A tree (10 m), (b) leaf initiation, (c), (e) seed (1.30), (d) leaf fall and seeds of Ficus palmata, (f) fruiting (30.45) (g) flowering.



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3.3. Fruit/Seed Characteristics

The color of the fruit in the first collection was light green in the 2nd week of April. The fruit turned dark purple at the final collection last May week [Table 2]. From initial to final collection, the fruit size ranged between 103.13 ± 5.37 (S1) and 502.26 ± 1.53 (S3) mm2 across all the sites. The seeds during the first two collections were extremely soft and immature. The mean seed size during the third collection ranged between 0.60 ± 0.03 (S2) and 1.06 ± 0.05 (S2) mm2 across all the sites.

Table 2: Variation in physical parameters of fruits of Ficus palmata over the collection period in Yr-1 (2017) and Yr-2 (2018) for site 1, site 2, and site 3.

SitesDOCCLRYr-1Yr-2


Fruit size mm2Weight of 100 fruits (g)No. of fruits in 100 gFruit size mm2Weight of 100 fruits (g)No. of fruits in 100 g
Site 111 AprilLG103.13±5.3743.30±0.85280.0±5.77106.68±0.8843.41±0.83260.00±5.77
18 AprilLG140.37±2.4661.50±0.31220.00±5.77141.70±6.0444.46±0.47270.00±8.82
25 AprilDG155.55±6.48115.83±1.53121.67±1.67152.58±1.2161.63±0.34173.33±8.82
02 MayP221.47±8.96136.97±8.8291.67±6.01201.20±5.70113.90±3.5183.33±3.33
09 MayP255.10±2.05155.83±3.0977.33±1.20227.99±7.24148.34±2.2057.67±0.88
16 MayDP386.45±1.23156.40±2.4873.67±2.03373.15±2.22158.07±4.1753.33±3.33
23 MayDP409.52±5.27157.17±1.9767.33±1.20397.38±1.76160.34±0.7443.33±3.33
Site 211 AprilLG112.56±4.1031.40±2.43323.33±3.33111.78±1.4831.67±2.66313.33±6.67
18 AprilLG174.90±6.6096.67±2.40213.33±3.33134.55±4.2243.87±0.41243.33±3.33
25 AprilDG199.76±7.61107.33±4.37121.00±0.58194.37±9.9695.37±4.68113.33±6.67
02 MayP263.20±1.17137.53±6.8797.00±1.53200.43±9.56109.93±0.2993.33±3.33
09 MayP301.77±5.01163.63±0.4384.67±2.40220.55±2.62121.25±4.6990.00±5.77
16 MayDP322.00±6.47167.70±0.1576.33±2.19312.33±3.13158.30±1.6753.33±3.33
23 MayDP413.47±9.84169.53±7.3569.67±0.33412.34±5.61160.23±3.5853.33±3.33
Site 311 AprilLG111.21±7.2531.73±2.60320.00±5.77106.41±4.0731.37±2.63306.67±6.67
18 AprilLG118.97±9.1643.07±0.09256.67±3.33110.20±4.1842.73±0.32246.67±3.33
25 AprilDG211.15±2.3695.47±3.09125.00±2.89204.40±9.7192.23±4.53133.33±3.33
02 MayP213.22±6.41114.07±3.34123.67±1.86216.34±2.75115.33±2.47113.33±3.33
09 MayP217.67±8.10141.27±0.07122.00±2.00232.91±3.94143.23±0.4193.33±3.33
16 MayDP342.16±5.23151.27±0.0770.00±0.00321.85±3.64152.83±1.5053.33±3.33
23 MayDP502.26±1.53162.30±2.5563.67±1.86414.80±3.61161.17±4.9050.00±0.58

DOC: Denotes date of collection, CLR: Color, DG: Dark green, LG: Light green, P: Purple, DP: Dark purple.

In both the years, the fruit size between initial to the final collection was 103.13 ± 5.37 and 409.52 ± 5.27mm2 throughout collection change in fruit size was 306.39 mm2, and the seed size between initial to the final collection was 0.81 ± 0.04 and 3.00 ± 0.04 throughout collection change in seed size was 2.19 mm2 at (S1). The fruit size between initial to the final collection was 111.78 ± 1.48 and 413.47 ± 9.84 mm2 over the period of collection change in fruit size was 301.69 mm2, and seed size between initial to the final collection was 0.60 ± 0.03 and 2.79 ± 0.12 over the period of collection change in seed size was 2.19 mm2 at (S2). The fruit size between initial to final collection was 106.41 ± 4.07 and 502.26 ± 1.53 mm2 over the period of collection change in fruit size was 395.85 mm2 and seed size between initial to final collection was 1.00 ± 0.05 and 2.44 ± 0.04 over the period of collection change in seed size was 1.44 mm2 at (S3).

At site 1 the weight of 100 fruits between initial to final collection was 43.30 ± 0.85 and 160.34 ± 0.74 g over the period of collection change in fruit weight was 117.04 g and weight of 100 seeds between initial to final collection was 0.07 ± 0.01 and 0.17 ± 0.01 g over the period of collection change in seed weight was 0.1 g. At site 2 the weight of 100 fruits between initial to final collection was 31.40 ± 2.43 and 169.53 ± 7.35 g over the period of collection change in fruit weight was 138.13 g and weight of 100 seeds between initial to final collection was 0.05 ± 0.01 and 0.25 ± 0.01 g over the period of collection change in seed weight was 0.2 g. At site 3 the weight of 100 fruits between initial to final collection was 31.37 ± 2.63 and 162.30 ± 2.55 g over the period of collection change in fruit weight was 130.93 g and weight of 100 seeds between initial to final collection was 0.06 ± 0.01 and 0.23 ± 0.01g over the period of collection change in seed weight was 0.17 g across both the years. Across all the sites and years the largest fruit size was in (S3) Yr-1. Across all the sites and years the heaviest fruit was recorded at (S2) Yr-1 [Tables 2,3]. Across all the sites and years the largest seed size was in (S1) Yr-2. Across all the sites the heaviest seed was recorded at (S2) Yr-1.

Table 3: Variation in physical parameters of seeds of Ficus palmata over the collection period in Yr-1 (2017) and Yr-2 (2018) for site 1, site 2, and site 3 (Im=Seeds were immature inside the fruit).

SitesDOCCLRYr-1Yr-2


Seed size mm2Weight of 100 seeds (g)No. of seeds in 100 gSeed size mm2Weight of 100 seeds (g)No. of seeds in 100 g
Site 111 AprilImImImImImImIm
18 AprilImImImImImImIm
25 AprilOW0.93±0.070.07±0.0186733.33±2.030.81±0.040.07±0.0286900.00±10.12
02 MayOW1.00±0.030.09±0.0194500.00±0.580.88±0.060.09±0.0194500.00±7.77
09 MayLB1.02±0.070.10±0.0195300.00±1.730.99±0.100.11±0.0197100.00±10.97
16 MayB2.36±0.030.13±0.0198600.00±4.932.25±0.070.12±0.0297700.00±12.17
23 MayB2.55±0.230.16±0.01210533.33±6.643.00±0.040.17±0.01119600.00±12.17
Site 211 AprilImImImImImImIm
18 AprilOW0.60±0.030.07±0.0175500.00±6.35ImImIm
25 AprilOW1.00±0.010.08±0.0176366.67±9.771.06±0.050.05±0.0176066.67±9.94
02 MayLB1.07±0.040.12±0.0186566.67±9.531.09±0.120.07±0.0181966.67±8.41
09 MayLB1.72±0.260.16±0.0195933.33±2.031.23±0.110.08±0.0185766.67±11.67
16 MayB2.35±0.110.18±0.0197600.00±6.931.54±0.180.11±0.0194500.00±11.02
23 MayB2.79±0.120.25±0.0198100.00±6.082.63±0.080.15±0.0196200.00±14.43
Site 311 AprilImImImImImImIm
18 AprilImImImImImImIm
25 AprilOW1.00±0.050.17±0.0185466.67±6.121.03±0.030.06±0.0185800.00±10.41
02 MayOW1.12±0.110.17±0.0193700.00±5.291.15±0.020.09±0.0186133.33±12.72
09 MayLB1.44±0.060.19±0.0196400.00±6.351.42±0.060.12±0.0194000.00±9.17
16 MayB2.44±0.030.22±0.02119600.33±7.541.76±0.160.14±0.0196333.33±6.64
23 MayB2.44±0.040.23±0.01120133.33±7.862.42±0.170.17±0.01210366.67±13.20

DOC: Denotes date of collection, CLR: Color, OW: Off-white, LB: Light brown, B: Brown.

Analysis of variance (ANOVA) showed that fruit size, weight of 100 fruits and number of fruits in 100 g varied significantly across years, sites and dates (P < 0.05). The interactions between year × site, year × date, site × date, and year × site × date were also significant for fruit size, weight of 100 fruits and number of fruits in 100 g. ANOVA showed that size, weight, and number of seeds in 100 g were significant across years and dates (P < 0.05). The interactions between year × site, year × date, site × date and year × site × date were significant for seed size, weight of 100 seeds, and number of seeds (P < 0.05) [Tables 4,5].

Table 4: Analysis of variance (ANOVA) for different fruit parameters across different collection dates (number), sites, and years of Ficus palmata.

CharactersSourceType III Sum of SquaredfMean SquareF-Value
Fruit size (mm2)Year12354.607112354.607102.605**
Site2033.22621016.6138.443**
Date1623433.4727231919.0671.926**
Year×site2644.48921322.24510.981**
Year×date6150.65461025.1098.514**
Site×date35470.172122955.84824.548**
Year×site×date30109.453122509.12120.838**
Weight of 100 fruits (g)Year4475.00614475.006148.906**
Site1512.9322756.46625.171**
Date301693.971743099.1391.434**
Year×site2563.15521281.57742.645**
Year×date2814.3756469.06215.608**
Site×date3114.91912259.5778.637**
Year×site×date4427.37412368.94812.277**
Number of fruits in 100 gYear672.0711672.07113.519**
Site4499.19022249.59545.251**
Date974341.5877139191.6552.800**
Year×site1023.8572511.92910.298**
Year×date7636.98461272.83125.603**
Site×date22033.365121836.11436.934**
Year×site×date7441.58712620.13212.474**

NS: Non significant,

Significant at 5% (P<0.05).

Table 5: Analysis of variance (ANOVA) for different seed parameters across different collection dates (number), sites, and years of Ficus palmata.

CharactersSourceType III sum of squaredfMean squareF-value
Seed size (mm2)Year0.47710.47718.193**
Site0.17920.0903.420NS
Date108.211715.459589.991**
Year×site0.45520.2288.690**
Year×date1.17960.1977.500**
Site×date1.984120.1656.311**
Year×site×date0.873120.0732.778**
Weight of 100 seeds (g)Year0.05510.055277.648**
Site0.02320.01257.752**
Date0.51570.074369.008**
Year×site0.02820.01469.161**
Year×date0.01460.00211.951**
Site×date0.020120.0028.157**
Year×site×date0.021120.0028.886**
Number of seeds in 100 gYear1.17211.1726.590**
Site2.06621.0335.809**
Date2.84474.0622.284**
Year×site3.22021.6109.052**
Year×date2.18563.6422.048**
Site×date2.344121.9531.098**
Year×site×date2.771122.3091.298**

NS: Non significant,

Significant at 5% (P<0.05).

Germination started from the third collection and varied from 0.09 ± 0.02 to 0.69 ± 0.30%. Germination rate increases with each collection and maximum germination occurred in seed of final collection. Maximum germination ranged between 84.68 ± 2.42 and 95.33 ± 1.64% when seed moisture content was between 36.33 ± 0.88 and 42.33 ± 0.88% [Figure 3].

Figure 3: Fruit/Seed Moisture content% and Germination% of Ficus palmata. (SMC denotes Seed Moisture Content, FMC: Fruit Moisture Content and GER: Germination).



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In both years germination of stored seed at room temperature declined after 3 months 10.42 ± 1.42% and 10.11 ± 1.09% and germination under room temperature decreased drastically after 60 days in both the years. In both years, there was no germination in seed stored in refrigerator after 6 months. The best temperature for storage was 1–3°C in refrigerator [Figure 4].

Figure 4: Germination% at room temperature and refrigerator of Ficus palmata.



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ANOVA showed that fruit and seed moisture content varied significantly across years, sites and dates (P < 0.05). The interaction between site × date, year × site, and year × site × date was significant for moisture content and germination of fruit and seed (P < 0.05) [Table 6].

Table 6: Analysis of variance (ANOVA) for fruit and seed moisture content and germination across different collection dates (number), sites, and years of Ficus palmata.

CharactersSourceType III sum of squaredfMean squareF-value
Fruit moisture content %Year283.4701283.47036.927**
Site256.3272128.16316.695**
Date26085.04373726.435485.431**
Year×site1273.0902636.54582.921**
Year×date39.11466.5190.849NS
Site×date534.1091244.5095.798**
Year×site×date429.7051235.8094.665**
Seed moisture content %Year283.2601283.26051.038**
Site111.274255.63710.025**
Date75637.651710805.3791.947**
Year×site174.383287.19115.710**
Year×date3707.1826617.864111.327**
Site×date5763.13712480.26186.534**
Year×site×date5539.66112461.63883.178**
Germination %Year184.5981184.59818.825**
Site633.8002316.90032.317**
Date162532.42723218.9182.368**
Year×site1170.6382585.31959.689**
Year×date331.275655.2135.630**
Site×date1363.05512113.58811.583**
Year×site×date1136.2841294.6909.656**

NS: Non significant,

Significant at 5% (P<0.05).

The germination was positively correlated with fruit size (r = 0.91; P < 0.05) [Figure 5], fruit weight (r = 0.85; P < 0.05) [Figure 6], and negatively correlated with fruit moisture content (r = 0.85; P < 0.05) [Figure 7] across all the sites. Similarly, germination was positively correlated with seed size (r = 0.90; P < 0.05) [Figure 8], seed weight (r = 0.77; P < 0.05) [Figure 9], and negatively correlated with seed moisture content (r = 0.85; P < 0.05) [Figure 10].

Figure 5: Relationship between fruit size and seed germination for Ficus palmata.



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Figure 6: Relatyonship between fruit weight nd seed germination for Ficus palmata.



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Figure 7: Relatyonship between fruit moisture content% and seed germination for Ficus palmata.



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Figure 8: Relatyonship between seed size and seed germination for Ficus palmata.



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Figure 9: Relatyonship between seed weight and seed germination for Ficus palmata.



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Figure 10: Relatyonship between seed moisture content % and seed germination for Ficus palmata.



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3.4. Nutritional Status

The mean moisture content, protein content, ash content, calcium, and phosphorous% of leaves were 18.30 ± 1.54, 4.41 ± 1.41, 6.44 ± 1.21, 1.02 ± 1.22, and 1.18 ± 1.02%. The mean moisture content, protein content, ash content, calcium, and phosphorous% of fruits was 58.49 ± 4.72, 11.15 ± 0.52, 11.45 ± 1.39, 1.56 ± 1.22, and 1.77 ± 1.26% [Table 7].

Table 7: Mean Moisture content%, Protein%, Ash%, Calcium%, and Phosphorous% of leaves and fruits of Ficus palmata.

SpeciesMoisture%Protein%Ash%Calcium%Phosphorous%
Ficus palmata
 Leaf18.30±1.544.41±1.416.44±1.211.02±1.221.18±1.02
 Fruit58.49±4.7211.15±0.5211.45±1.391.56±1.221.77±1.26

4. DISCUSSION

F. palmata is a lesser-known species, and the nutritional value of species is also not very well defined. Ficus species produce a large amount of fruit and seed, but the distribution of the selected species in the natural condition is restricted to small pockets. Fruit of F. palmata is edible for animals and humans; thus, they are collected extensively before maturation resulting in curtailed dispersal, regeneration, and germination. Very little information is available on the seed germination of the selected species, along with the fruit/seed maturation time. The timing of phenological events, mostly flowering, fruiting, seed fall, etc., is relatively less studied particularly in relation to changing climate.

4.1. Regeneration

Complete absence of seedlings and saplings in a forest indicates no regeneration [10]. Lack of sufficient regeneration is a major problem for mountain forests [23]. In the present study, F. palmata showed scattered distribution and low tree density. Seedlings were completely absent in all the studied sites. Saplings were present in all selected sites except site 1 but the density was low (22 to 67 ind/ha). Similarly, Jyotsna et al. [24] have reported the absence of seedlings and saplings of F. roxburghii in study areas of the Nainital district. Regeneration of species is dependent on internal community processes and exogenic disturbance [25-27]. reported F. vasta Forssk. and F. thonningii Blume. in not regenerating category. However, in Hazarikhil Wildlife Sanctuary, Bangladesh F. hispida Linn. (792 per ha) showed the highest number of seedlings and F. religiosa L. 408 seedlings per ha [28]. The absence of anthropogenic pressure appears to be the major cause of good regeneration. In wild edible plants availability of mature seed is always been a big problem. The poor natural regeneration of Ficus species indicates that seed sources are depleted through harvesting of immature and mature fruits. However, Malik et al. [10] have reported absence of seedlings and low saplings density in F. roxburghii in a protected area and its adjoining areas in Western Himalaya.

4.2. Phenology

The phenology of Ficus in relation to other forest trees have been less studied. Ficus species show various fruiting phenological patterns. The leaf changes can occur seasonally [29]. When we compare the findings of present study on phenological events of F. palmata with earlier studies we find that there is a paucity of information and very few studies have been conducted previously. There was very little variation in the timing of seed fall and leaf fall but leaf initiation was delayed by 1 month in comparison to earlier records in the present study. Most of the previous studies have shown flowering time between March and April but in the present study it was delayed by about 1 month and started from April, [7] has reported flowering between May and June. As per the available literature on F. palmata fruiting took place in the rainy season (July–August) and only once in a year but in present study fruiting was observed twice a year in March–May and October–December.

4.3. Seed Maturation

Color change is always considered a reliable indicator of maturity. In the present study, the color change of fruit from light green to dark purple in F. palmata appeared to be an important indicator of maturity. Diba et al. [30] reported the fruit color of Ficus sur changed from light yellow to pale brown at maturation. Moisture decline from maturing seeds is closely connected to maturity [31]. Lavania et al. [32] reported the moisture content decreased with development of maturity in Acacia nilotica. In the present study, maximum germination occurred when seed moisture content was between 35.02 and 42.33% in F. palmata. Similarly maximum germination was observed when the moisture content had declined in these species of Ficus such as F. krishnae and F. lundellii [33,34].

In the present study, the correlation between fruit/seed moisture content was negatively correlate with seed germination. Similarly in Myrica esculenta [35] found that correlation between seed moisture content and germination was negative. Tewari and Tewari [36] also reported the negative correlation between seed moisture content and germination in P. cerasoides in A. indica by [37].

4.4. Nutritive Value

During winter animal loose their body weight and milk production drops drastically when animals are mainly provided with fodder tree leaves and rice straw. This problem may be due to deciduous plants and composition and availability of nutrients during moisture stress condition. Protein, phosphorus, and calcium are very important for milk producing animals [38]. Ficus species are the main fodder tree species that are lopped during summer season to feed the animals [39]. In the present study, it was observed that value of ash content, protein, and calcium except phosphorous of leaf of F. palmata was relatively high compared to other species [40]. However, in F. polita ash and protein were higher compared to the present study in F. palmata.


5. CONCLUSION

The change in fruit color and range of moisture content of seeds when maximum germination occurs appears to be reliable physical indicators of fruit/seed maturity. However, we know very little about the adaptation traits of tree species about their reproductive phenology and germination behavior. How the species will respond to a warming climate and what will be its effect on its seed traits and on seeds on the ground needs further investigations. Most needed are studies on these lesser known wild tree species to understand the possible effects of climate change on such species that already occur in small pockets with low densities.


6. ACKNOWLEDGMENT

The authors are thankful to Head of the Department of Forestry and Environmental Science, D. S. B. Campus, Kumaun University, Nainital for providing the laboratory facilities.


7. AUTHORS’ CONTRIBUTIONS

All authors made substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; took part in drafting the article or revising it critically for important intellectual content; agreed to submit to the current journal; gave final approval of the version to be published; and agreed to be accountable for all aspects of the work. All the authors are eligible to be an author as per the International Committee of Medical Journal Editors (ICMJE) requirements/guidelines.


8. FUNDING

There is no funding to report.


9. CONFLICTS OF INTEREST

The authors do not have any conflicts of interest.


10. ETHICAL APPROVALS

This study does not involve experiments on animals or human subjects.


11. DATA AVAILABILITY

Tha data will be provided and made available as per the genuine interest and as per the journal policy.


12. PUBLISHER’S NOTE

This journal remains neutral with regard to jurisdictional claims in published institutional affiliation

REFERENCES

1.  Mathew G, Skaria BP, Joseph A. Standardization of conventional propagation techniques for four medicinal species of genus Ficus Linn. Indian J Nat Prod Resour 2011;2:88-96.

2.  Corner EJ. Check-list of Ficus in Asia and Australiasia with keys to identification the gardens. Bull Singapore 1965;21:1-186.

3.  Berg CC. Classification and distribution of Ficus. Experientia 1989;45:605-11. [CrossRef]

4.  Berg CC. Flora Malesiana precursor for the treatment of Moraceae 3:Ficus subgenus Ficus. Blumea J Plant Taxonomy Plant Geogr 2003;48:529-50. [CrossRef]

5.  Chaudhary LB, Sudhakar JV, Srivastava A, Bajpai O, Tiwari R, Murthy GV. Synopsis of the genus Ficus L. (Moraceae) in India. Taiwania 2012;57:193-216.

6.  Shanahan M, SO S, Compton SG, Corlett R. Fig-eating by vertebrate frugivore:A global review. Biol Rev Camb Philos Soc 2001;76:529-72. [CrossRef]

7.  Mewar D, Nautiyal MC, Naithani DC. Effect of various seed treatment on seed germination parameters in wild fig (Ficus palmate I). Int J Curr Res 2017;9:47834-6.

8.  Pramanick DD. A synoptic account of the family Moraceae in Uttarakhand. eJournal Appl For Ecol 2017;5:17-26.

9.  Saklani S, Chandra S. Phytochemical screening of Garhwal Himalaya wild edible fruit Ficus palmata. Int J Pharm Tech Res 2012;4:1185-91.

10.  Malik ZA, Youssouf M, Singh S, Bhatt AB. Tree regeneration status and population structure along the disturbance gradient (A case study from Western Himalaya). ENVIS Bull Himalayan Ecol 2017;25:81-93.

11.  Saxena AK, Singh JS. Tree population structure of certain Himalayan forest associations and implications concerning their future composition. Vegetatio 1984;58:61-9. [CrossRef]

12.  Ralhan PK, Saxena AK, Singh JS. Analysis of forest vegetation at and around Nainital in Kumaun Himalaya. Proc Indian Natl Sci Acad 1982;1:121-37.

13.  Malik ZA, Bhatt AB. Regeneration status of tree species and survival of their seedlings in Kedarnath Wildlife Sanctuary and its adjoining areas in Western Himalaya, India. Trop Ecol 2016;57:677-90.

14.  Singh N, Ram J, Tewari A, Yadav RP. Phenological events along the elevation gradient and effect of climate change on Rhododendron arboretum Sm. in Kumaun Himalaya. Curr Sci 2015;108:106-10.

15.  International Seed Testing Association. International rules for seed testing association seed science and technology Moisture content and equipment Wkg Group. In:Report of the Forest Tree Seed Committee. Seed Science and Technology. Vol. 9. Switzerland:International Seed Testing Association;1981. 29-32.

16.  Tamta KK, Tewari A. Indicators of seed maturation in Prunus armenica L. in Indian Himalayan region. Int J Res Anal Rev 2018;5:860-6.

17.  Shah S, Tewari A. Limited impact of climate change on seed maturation time in Myrica esculenta Buch-Ham. Ex. D. Don in Himalayan region. Int J Environ Agric Biotechnol 2016;1:713-7. [CrossRef]

18.  Snedecor GW, Cochran WG. Statistical Methods. 6th ed. New Delhi:Oxford and IBH;1967.

19.  Tewari B, Tewari A. Capsule maturation timing in Rhododendron arboretum simth in the Central Himalayan region. Indian J Ecol 2019;46:768-71.

20.  Magomya AM, Kubmarrawa D, Ndahi JA, Yebpella GG. Determination of plant protein via the kjeldal method and amino acid analysis:A comparative study. Int J Sci Technol Res 2014;3:68-72.

21.  Bhogaonkar PY, Chavhan VN, Kanerkar UR. Nutritional potential of Ficus racemosa L. Fruits. Biosci Discov 2014;5:150-3.

22.  Khan MR, Darwaish AM, Tahir U. Sodium, potassium, iron, calcium and phosphorous content of some Pakistani condiments. Sci Inq Rev 2018;2:16-22. [CrossRef]

23.  Krauchii N, Brang P, Schonenberger W. Forests of mountainous regions:Gaps in knowledge and research needs. For Ecol Manage 2000;132:73-82. [CrossRef]

24.  Jyotsna, Tewari A, Shah S, Tamta KK, Singh N. Fruit maturation and germination in Ficus auriculata Lour. A lesser known multipurpose tree species in Kumaun Himalayan region. Ecol Environ Conserv 2020;26:142-7.

25.  Baker PC, Patrik JB. Phyllocaladus asplenifolius variability in the population structure of the regeneration niche and dispersion pattern in Tasmanian forest. Aust J Bot 1994;42:136-90. [CrossRef]

26.  Chauhan DS, Singh CS, Chauhan S, Todaria NP, Khalid MA. Regeneration and tree diversity in natural and planted forests in a terai-bhabhar forest in Katarniaghat Wildlife Sanctuary, India. Trop Ecol 2008;49:53-67.

27.  Bogale T, Datiko D, Belachew S. Structure and natural regeneration status of woody plants of berbere afromontane Moist forest, Bale zone, South East Ethiopia, implication to biodiversity conservation. Open J For 2017;7:352-71. [CrossRef]

28.  Rahman MA, Alim MA, Hossain MK, Hossain MA. Prospect of natural regeneration of tree species in Hazarikhil Wildlife Sanctuary of Chattogram, Bangladesh. J Biodivers Conserv Bioresour Manage 2019;5:1-12. [CrossRef]

29.  Bianchini E, Emmerick JM, Messetti AV, Pimenta JA. Phenology of two Ficus species in seasonal semi-deciduous forest in Southern Brazil. Braz J Biol 2015;75:206-14. [CrossRef]

30.  Diba D, Bultosa G, Tolesa GN. Effect of maturity stages on nutritive quality and sensory properties of Fig fruits. Botsw J Agric Appl Sci 2017;12:15-22.

31.  Pandit A, Pant K, Ram J. Effect of collection date on capsule moisture content and germination of Populus ciliata wall-ex. Rayole from Central Himalaya. New For 2002;23:121-30. [CrossRef]

32.  Lavania P, Singh RP, Tewari A, Sharma HK. Studies on seed maturity indices of Acacia nilotica in Uttar Pradesh. J Pharmacogn Phytochem 2018;7:192-5.

33.  Kumar AC, Chitra CR, Bindu S, Padmesh P. Seed germination and storage studies in Ficus krishnae C. DC. Indian J Plant Physiol 2008;13:66-72.

34.  Garcia X, Hong TD, Ellis RH. Seed dormancy and germination of Ficus lundellii and tropical forest restoration. Tree Physiol 2005;26:81-5. [CrossRef]

35.  Shah S. Regeneration and Nursery Techniques of Myrica esculanta (Thesis). Uttarakhand:Department of Forestry Kumaun University Nainital;2005. 1-146.

36.  Tewari B, Tewari A. Seed germination in Prunus cerasoides D. Don influenced by influenced by natural seed desiccation and varying temperature in Central Himalayan region of Uttarakhand, India. Int J Bioassays 2016;5:4567-72. [CrossRef]

37.  Majeed M, Khan MA, Mughal AH, Bashir A. Maturity indices of Indian horse-chestnut (Aesculus indica Colebr) seeds under temperate Kashmir conditions. Silva Lusitana 2009;17:211-9.

38.  Osti NP, Chapagain PB, Tiwari MR, Upreti CR. Digestibility of Ficus roxburghii, Castanopsis indica and Ficus cunia on Growing Buffalo from Western Hills of Nepal. Nepal Agric Res J 2009;9:94-8. [CrossRef]

39.  Nautiyal M, Tiwari JK, Rawat DS. Exploration of some important fodder plans of Joshimath area of Chamoli district of Garhwal, Uttarakhand. Curr Bot 2017;8:144-9. [CrossRef]

40.  Joshi Y, Joshi AK, Prasad N, Juyal D. A review on Ficus palmata (Wild Himalayan Fig). J Phytopharmacol 2014;3:374-7. [CrossRef]

Reference

1. Mathew G, Skaria BP, Joseph A. Standardization of conventional propagation techniques for four medicinal species of genus Ficus Linn. Indian J Nat Prod Resour 2011;2:88-96.

2. Corner EJ. Check-list of Ficus in Asia and Australiasia with keys to identification the gardens. Bull Singapore 1965;21:1-186.

3. Berg CC. Classification and distribution of Ficus. Experientia 1989;45:605-11. https://doi.org/10.1007/BF01975677

4. Berg CC. Flora Malesiana precursor for the treatment of Moraceae 3: Ficus subgenus Ficus. Blumea J Plant Taxonomy Plant Geogr 2003;48:529-50. https://doi.org/10.3767/000651903X489537

5. Chaudhary LB, Sudhakar JV, Srivastava A, Bajpai O, Tiwari R, Murthy GV. Synopsis of the genus Ficus L. (Moraceae) in India. Taiwania 2012;57:193-216.

6. Shanahan M, SO S, Compton SG, Corlett R. Fig-eating by vertebrate frugivore: A global review. Biol Rev Camb Philos Soc 2001;76:529-72. https://doi.org/10.1017/S1464793101005760

7. Mewar D, Nautiyal MC, Naithani DC. Effect of various seed treatment on seed germination parameters in wild fig (Ficus palmate I). Int J Curr Res 2017;9:47834-6.

8. Pramanick DD. A synoptic account of the family Moraceae in Uttarakhand. eJournal Appl For Ecol 2017;5:17-26.

9. Saklani S, Chandra S. Phytochemical screening of Garhwal Himalaya wild edible fruit Ficus palmata. Int J Pharm Tech Res 2012;4:1185-91.

10. Malik ZA, Youssouf M, Singh S, Bhatt AB. Tree regeneration status and population structure along the disturbance gradient (A case study from Western Himalaya). ENVIS Bull Himalayan Ecol 2017;25:81-93.

11. Saxena AK, Singh JS. Tree population structure of certain Himalayan forest associations and implications concerning their future composition. Vegetatio 1984;58:61-9. https://doi.org/10.1007/BF00044928

12. Ralhan PK, Saxena AK, Singh JS. Analysis of forest vegetation at and around Nainital in Kumaun Himalaya. Proc Indian Natl Sci Acad 1982;1:121-37.

13. Malik ZA, Bhatt AB. Regeneration status of tree species and survival of their seedlings in Kedarnath Wildlife Sanctuary and its adjoining areas in Western Himalaya, India. Trop Ecol 2016;57:677-90.

14. Singh N, Ram J, Tewari A, Yadav RP. Phenological events along the elevation gradient and effect of climate change on Rhododendron arboretum Sm. in Kumaun Himalaya. Curr Sci 2015;108:106-10.

15. International Seed Testing Association. International rules for seed testing association seed science and technology Moisture content and equipment Wkg Group. In: Report of the Forest Tree Seed Committee. Seed Science and Technology. Vol. 9. Switzerland: International Seed Testing Association; 1981. p. 29-32.

16. Tamta KK, Tewari A. Indicators of seed maturation in Prunus armenica L. in Indian Himalayan region. Int J Res Anal Rev 2018;5:860-6. 17. Shah S, Tewari A. Limited impact of climate change on seed maturation time in Myrica esculenta Buch-Ham. Ex. D. Don in Himalayan region. Int J Environ Agric Biotechnol 2016;1:713-7. https://doi.org/10.22161/ijeab/1.4.13

18. Snedecor GW, Cochran WG. Statistical Methods. 6th ed. New Delhi: Oxford and IBH; 1967.

19. Tewari B, Tewari A. Capsule maturation timing in Rhododendron arboretum simth in the Central Himalayan region. Indian J Ecol 2019;46:768-71.

20. Magomya AM, Kubmarrawa D, Ndahi JA, Yebpella GG. Determination of plant protein via the kjeldal method and amino acid analysis: A comparative study. Int J Sci Technol Res 2014;3:68-72.

21. Bhogaonkar PY, Chavhan VN, Kanerkar UR. Nutritional potential of Ficus racemosa L. Fruits. Biosci Discov 2014;5:150-3.

22. Khan MR, Darwaish AM, Tahir U. Sodium, potassium, iron, calcium and phosphorous content of some Pakistani condiments. Sci Inq Rev 2018;2:16-22. https://doi.org/10.32350/sir/21/020103

23. Krauchii N, Brang P, Schonenberger W. Forests of mountainous regions: Gaps in knowledge and research needs. For Ecol Manage 2000;132:73-82. https://doi.org/10.1016/S0378-1127(00)00382-0

24. Jyotsna, Tewari A, Shah S, Tamta KK, Singh N. Fruit maturation and germination in Ficus auriculata Lour. A lesser known multipurpose tree species in Kumaun Himalayan region. Ecol Environ Conserv 2020;26:142-7.

25. Baker PC, Patrik JB. Phyllocaladus asplenifolius variability in the population structure of the regeneration niche and dispersion pattern in Tasmanian forest. Aust J Bot 1994;42:136-90. https://doi.org/10.1071/BT9940163

26. Chauhan DS, Singh CS, Chauhan S, Todaria NP, Khalid MA. Regeneration and tree diversity in natural and planted forests in a terai-bhabhar forest in Katarniaghat Wildlife Sanctuary, India. Trop Ecol 2008;49:53-67.

27. Bogale T, Datiko D, Belachew S. Structure and natural regeneration status of woody plants of berbere afromontane Moist forest, Bale zone, South East Ethiopia, implication to biodiversity conservation. Open J For 2017;7:352-71. https://doi.org/10.4236/ojf.2017.73021

28. Rahman MA, Alim MA, Hossain MK, Hossain MA. Prospect of natural regeneration of tree species in Hazarikhil Wildlife Sanctuary of Chattogram, Bangladesh. J Biodivers Conserv Bioresour Manage 2019;5:1-12. https://doi.org/10.3329/jbcbm.v5i2.44909

29. Bianchini E, Emmerick JM, Messetti AV, Pimenta JA. Phenology of two Ficus species in seasonal semi-deciduous forest in Southern Brazil. Braz J Biol 2015;75:206-14. https://doi.org/10.1590/1519-6984.10614

30. Diba D, Bultosa G, Tolesa GN. Effect of maturity stages on nutritive quality and sensory properties of Fig fruits. Botsw J Agric Appl Sci 2017;12:15-22.

31. Pandit A, Pant K, Ram J. Effect of collection date on capsule moisture content and germination of Populus ciliata wall-ex. Rayole from Central Himalaya. New For 2002;23:121-30. https://doi.org/10.1023/A:1015694310479

32. Lavania P, Singh RP, Tewari A, Sharma HK. Studies on seed maturity indices of Acacia nilotica in Uttar Pradesh. J Pharmacogn Phytochem 2018;7:192-5.

33. Kumar AC, Chitra CR, Bindu S, Padmesh P. Seed germination and storage studies in Ficus krishnae C. DC. Indian J Plant Physiol 2008;13:66-72.

34. Garcia X, Hong TD, Ellis RH. Seed dormancy and germination of Ficus lundellii and tropical forest restoration. Tree Physiol 2005;26:81-5. https://doi.org/10.1093/treephys/26.1.81

35. Shah S. Regeneration and Nursery Techniques of Myrica esculanta (Thesis). Uttarakhand: Department of Forestry Kumaun University Nainital; 2005. p. 1-146.

36. Tewari B, Tewari A. Seed germination in Prunus cerasoides D. Don influenced by influenced by natural seed desiccation and varying temperature in Central Himalayan region of Uttarakhand, India. Int J Bioassays 2016;5:4567-72. https://doi.org/10.21746/ijbio.2016.05.007

37. Majeed M, Khan MA, Mughal AH, Bashir A. Maturity indices of Indian horse-chestnut (Aesculus indica Colebr) seeds under temperate Kashmir conditions. Silva Lusitana 2009;17:211-9.

38. Osti NP, Chapagain PB, Tiwari MR, Upreti CR. Digestibility of Ficus roxburghii, Castanopsis indica and Ficus cunia on Growing Buffalo from Western Hills of Nepal. Nepal Agric Res J 2009;9:94-8. https://doi.org/10.3126/narj.v9i0.11646

39. Nautiyal M, Tiwari JK, Rawat DS. Exploration of some important fodder plans of Joshimath area of Chamoli district of Garhwal, Uttarakhand. Curr Bot 2017;8:144-9. https://doi.org/10.19071/cb.2017.v8.3265

40. Joshi Y, Joshi AK, Prasad N, Juyal D. A review on Ficus palmata (Wild Himalayan Fig). J Phytopharmacol 2014;3:374-7. https://doi.org/10.31254/phyto.2014.3511

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