Termite occurrence
Overall, termite species belonging to four genera (Odontotermes, Coptotermes, Microtermes, and Heterotermes) representing two families (Rhinotermitidae and Termitidae) were recorded on trees in Bagh-e-Jinnah, Canal vegetation, Race-course Park, Model Town Park, Jallo forestry, and FC College botanical garden. Based on morphological features, this study recognized the higher termites Odontotermes obesus Rambur and Microtermes obesi Holmgren. They have frequently collected from mud plaster and galleries the bark of tree trunk. In contrast, the lower termites Coptotermes heimi and Heterotermes indicola Wasmann were collected from internal tree nest galleries and mud tube trials in both living and dead standing trees (Fig 2). A total of >7451 termite individuals were logged from all six habitats of district Lahore metropolitan area from 2019-20, with the relative abundance of O. obesus, C. heimi, H. indicola, and M. obesi was 47, 36, 16, and 1% in overall study areas respectively (Fig. 2). Canal and Bagh-e-Jinnah had significantly (P < 0.05; df = 6; F-value = 68.84) higher species abundance of both lower and higher termites as compared to Race-course Park, Model Town Park, Jallo forestry, and FCCU botanical garden (Supplementary Table 1). In collected termite species from all sampling sites, O. obesus were high in number all vegetation sites; however, the frequency of tree damage was caused by C. heimi followed by H. indicola.
The results of some general diversity indices including Dominance (D), Simpson (1-D), Shannon (H'), Evenness (e^H/S), Brillouin, Equitability (J), Fisher alpha (α), and Berger-Parker (B.P.) for each termite species were determined as shown in Table 1. Termite species C. heimi and H. indicola had moderately high dominance (D) that was 0.614 and 0.552, respectively, than O. obesus and M. obesi (0.343 and 0.209) in all surveyed parks. Likewise, C. heimi and H. indicola had significantly lowest (0.385 and 0.448) Simpson index (1-D), representing high diversity. In contrast, high values (0.790 and 0.675) of the Simpson index for M. obesi and O. obesus were observed, respectively, indicating the low diversity in the respected study area. Shannon index (entropy) was recorded 1.584, 1.366, 0.857, and 0.828 for M. obesi, O. obesus, H. indicola and C. heimi, respectively. Same patterns (M. obesi > O. obesus > H. indicola > C. heimi) were observed in the Evenness, Brillouin, and Equitability indices. Berger-Parker (B.P.) index was 774 and 718 for C. heimi and H. indicola, respectively, which is higher than the B.P. index (0.527 and 0.261) of O. besus and M. obesi as shown in Table 1.
Table 1. Diversity indices Dominance (D), Simpson (1-D), Shannon (H'), Evenness (e^H/S), Brillouin, Equitability (J), Fisher alpha (α), and Berger-Parker (B.P.) for each termite species in sampling sites.
Diversity indices
|
Termite species
|
t-statistics
|
p-Value
|
O. obesus
|
H. indicola
|
C. heimi
|
M. obesi
|
Taxa_(S)
|
6
|
4
|
5
|
5
|
0.52156
|
p > 0.01
|
Individuals
|
3780
|
718
|
2524
|
429
|
0.361066
|
p > 0.01
|
Dominance_(D)
|
0.343
|
0.552
|
0.6148
|
0.2098
|
0.447725
|
p > 0.05
|
Simpson_(1-D)
|
0.657
|
0.448
|
0.3852
|
0.7902
|
0.447725
|
p > 0.05
|
Shannon_(H)
|
1.366
|
0.8573
|
0.8285
|
1.584
|
0.428518
|
p > 0.05
|
Evenness_(e^H/S)
|
0.6532
|
0.5892
|
0.458
|
0.9749
|
0.387678
|
p > 0.05
|
Brillouin
|
1.361
|
0.8452
|
0.8233
|
1.557
|
0.432901
|
p > 0.05
|
Equitability (J)
|
0.7623
|
0.6184
|
0.5148
|
0.9842
|
0.422245
|
p > 0.05
|
Fisher_alpha (α)
|
0.6979
|
0.5587
|
0.5991
|
0.7945
|
0.315449
|
p > 0.05
|
Berger-Parker (BP)
|
0.5278
|
0.7187
|
0.7746
|
0.2611
|
0.377423
|
p > 0.05
|
The kernel density function for the distribution of termite in surveyed areas indicated that canal vegetation, Bagh-e-Jinnah and Racecourse park had higher and normal distribution than F.C. College, Model town park, and Jallo park, respectively, as shown in Figure 3.
Damage Assessment
The percentage and number of trees attacked by termites in district Lahore study sites varied by tree cluster (exotic or native) and region (Fig. 4). In the current survey, overall, 1290 trees to species level in six different vegetations were examined, out of which 290(22%) specimens were severely damaged by termite attack. The canal plantation, which was mostly comprised of exotic tree species, out of a total of 425 inspected tree species, 114(39.31%) exotic and 8(2.75%) native tree species were highly infested by termites. Whereas, in Bagh-e-Jinnah, out of a total of 294 inspected trees, 47(16%) native and only 5(1.7%) exotic tree species were damaged by termite attack (Fig. 4). Similarly, in Jallo forestry and Race-course park, 180 and 160 trees were inspected, 21(7.24%) native & 5(1.72%) exotic and 18(6.25%) native & 7(2.41%) exotic trees species were damaged by termites, respectively. The minimum termite infestation was observed in Model town park and F.C. College vegetations, where a total of 130 and 101 trees inspected, only 17(5.83%) native & 6(2.07%) exotic in Model town park and 20(6.89%) native & 3(1.03%) exotic tree species were attacked by termites (Fig. 4).
Exotic and native tree clusters characterize all surveyed parks. In exotic species, Populus euramericana, Hibiscus rosa Alstonia scholaris, Albizia porecera, Grevillea robusta, Jacaranda mimosifolia, and Delonix regia were included. Whereas, Acacia nilotica, Aegle marmelos, Albizia lebbeck, Azadirachta indica, Bambusa vulgaris, Bauhinia variegata, Butea frondosa, Cassia fistula, Dalbergia sissoo, Erythrina subrosa, Ficus religiousa, Heterophragma adenophyllum, Melia azedarach, Morus alba, Pinus roxburghii, and Thuja accidentials were indigenous tree species (Table 2).
Termite abundance and palatability of different tree species were varied among termite species. Populus euramericana and Morus alba were most susceptible against all termite species. Whereas, Cassia fistula, Grevellia robusta, Eagle marmelos, Ficus religiousa, Acacia nilotica, Artocarpus integrifolia, Bombax malabaricum, Callistemon citrinus, Chukrasia tabularis, Citharexylum sipnosum, Erthrina suberosa, Eucalyptus citriodora, Gleditsia triacathos Phylllanthus emblica, Platanus orientalis, and Polyathia longifolia were the least preferable against all termites species (Supplementary Table. 2).
Significant variations in infested trees were calculated within surveyed localities, evident that termites' attacks on trees vary as well as localities (Supplementary Fig 1). The results of the visual tree assessment indicated that an exotic tree species, P. euramericana had severe damage with the absolute frequency of 145 and 50% relative frequency by all termite species.
Table 2. Visual tree damage assessment with an absolute and relative frequency of the indigenous and native trees in the six different Lahore city parks of Punjab, Pakistan.
Tree clusters
|
Tree names
|
No attack
|
Low damage
|
Moderate
Damage
|
High damage
|
Very High damage
|
Absolute frequency (n)
|
Relative frequency (%)
|
Indigenous
|
Eagle marmelos
|
9
|
1
|
0
|
0
|
0
|
01
|
0.34
|
Albizzia lebbeck
|
27
|
4
|
0
|
0
|
0
|
04
|
1.37
|
Azadirachta indica
|
30
|
3
|
0
|
0
|
0
|
03
|
1.03
|
Bambus sp.
|
25
|
4
|
0
|
0
|
0
|
04
|
1.37
|
Bauhinia variegata
|
30
|
0
|
9
|
0
|
0
|
09
|
3.10
|
Acacia nilotica
|
42
|
3
|
5
|
0
|
0
|
08
|
2.70
|
Butea frondosa
|
45
|
1
|
3
|
8
|
5
|
17
|
5.86
|
Cassia fistula
|
43
|
1
|
0
|
0
|
0
|
01
|
0.34
|
Dalbergia sissoo
|
65
|
5
|
9
|
3
|
0
|
17
|
5.87
|
Erythrina suberosa
|
72
|
7
|
5
|
10
|
0
|
22
|
7.58
|
Ficus religiousa
|
15
|
1
|
0
|
0
|
0
|
01
|
0.34
|
Heterophragma adenophyllum
|
39
|
0
|
7
|
2
|
0
|
09
|
3.10
|
Melia azedarach
|
45
|
2
|
2
|
0
|
0
|
04
|
1.37
|
Morus alba
|
62
|
0
|
7
|
10
|
8
|
25
|
8.62
|
Pinus roxburghii
|
20
|
4
|
0
|
0
|
0
|
4
|
1.37
|
Thuja occidentialis
|
21
|
2
|
0
|
0
|
0
|
2
|
0.68
|
Exotic
|
Populus euramericana
|
255
|
4
|
30
|
85
|
26
|
145
|
50.00
|
Hibiscus rosa
|
10
|
0
|
0
|
1
|
0
|
1
|
0.34
|
Alstonia scholaris
|
42
|
3
|
2
|
0
|
0
|
5
|
1.72
|
Albizzia procera
|
22
|
2
|
0
|
0
|
0
|
2
|
0.68
|
Grevillea robusta
|
24
|
0
|
1
|
0
|
0
|
1
|
0.34
|
Jacaranda ovalifolia
|
36
|
3
|
0
|
0
|
0
|
3
|
1.03
|
Delonix regia
|
21
|
2
|
0
|
0
|
0
|
2
|
0.68
|
Total
|
|
1000
|
52
|
80
|
119
|
39
|
290
|
100
|
However, the damage frequency of all other tree species by termite infestation was significantly less than, except M. alba a native tree species, was highly damage by termites' attack with 8.62% relative frequency and 25 absolute frequency (n). Minimum visual tree damage among exotic species was observed in Grevillea robusta, Hibiscus rosa, Albizzia. procera, and Delonix regia, while Eagle marmelos, Cassia fistula, Ficus religiosa and Thuja accidentialis had minimum termite damage frequency among native tree species.
Table 3. Multivariate analysis for the main effects and interactions of regressors including tree diameter breast height, tree clusters (exotic/native), and tree status (dead/living) concerning termite infestation
Parameter
|
Variable's categories
|
D.F.
|
Estimate
|
Standard Error
|
95% Confidence Limits
|
Wald Chi-Square
|
Pr > Chi Sq
|
Intercept1
|
|
|
1
|
1.0668
|
0.1358
|
0.8007-1.3329
|
61.75
|
0.000
|
DBH
|
|
|
1
|
-0.1242
|
0.0177
|
-0.1590-0.0895
|
49.09
|
0.000
|
Tree cluster
|
Exotic
|
|
1
|
0.8145
|
0.1967
|
0.4291-1.2000
|
17.15
|
0.000
|
Tree cluster
|
Native
|
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
Tree status
|
Dead
|
|
1
|
-1.5315
|
0.3626
|
-2.2422-0.8208
|
17.84
|
0.000
|
Tree status
|
Live
|
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
DBH*Tree cluster*Tree status
|
Exotic
|
Live
|
1
|
-0.0037
|
0.0295
|
-0.0617-0.0542
|
0.02
|
0.899
|
DBH*Tree cluster*Tree status
|
Exotic
|
Dead
|
1
|
-0.0434
|
0.0155
|
-0.0737-0.0131
|
7.88
|
0.005
|
DBH*Tree cluster*Tree status
|
Native
|
Dead
|
1
|
-0.0643
|
0.0439
|
-0.1503-0.0217
|
2.14
|
0.143
|
DBH*Tree cluster*Tree status
|
Native
|
Live
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
DBH*Tree cluster
|
Exotic
|
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
DBH*Tree cluster
|
Native
|
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
DBH*Tree status
|
Dead
|
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
DBH*Tree status
|
Live
|
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
Tree cluster*Tree status
|
Exotic
|
Dead
|
1
|
-0.2256
|
0.5458
|
-1.2954-0.8442
|
0.17
|
0.679
|
Tree cluster*Tree status
|
Exotic
|
Live
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
Tree cluster*Tree status
|
Native
|
Dead
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
Tree cluster*Tree status
|
Native
|
Live
|
0
|
0.0000
|
0.0000
|
0.0000-0.0000
|
.
|
.
|
DBH*DBH
|
|
|
1
|
0.0022
|
0.0004
|
0.0015-0.0029
|
35.45
|
0.000
|
Scale
|
|
|
0
|
1.0000
|
0.0000
|
1.0000-1.0000
|
|
|
Termite-Tree Interactions
Interaction between tree features (tree diameter up to breast height, tree clusters (exotic/native), and tree status (dead/living)) and termite infestation has been observed, as shown in table 3. There were significant main effects of DBH (χ 2 = 49.09, P = 0.000), tree status, if the tree is dead (χ2 = 17.15, P = 0.000) and tree cluster if tree is exotic (χ 2 = 17.84, P = 0.000) on termite infestation. Whereas no significant interaction was observed among DBH, tree cluster, and tree status regarding the termite infestation, except the interaction between DBH, exotic tree cluster type, and living tree status showed a significant effect (χ 2 = 7.88, P = 0.005) on termite infestation (Table 3).
Foraging Ecology of Termites
High termite occurrence was affected by different factors such as tree diameter, termite species and climatic factors. Termite abundance was positively and significantly correlated (r = 0.994; P < 0.05) with the diameter of standing trees up to breast height (Fig 5). The correlation analysis of termite abundance with climatic factors indicated that foraging subterranean termites O. obesus, C. heimi, H. indicola and M. obesi observed to be more reliant on temperature and rainfall than reality humidity, as shown in Table 4.
No significant infestation by any termite species was observed in the winter season months when the temperature was minimum (January, February, March, and December). In contrast, the relative humidity was noted high (Fig. 6). However, when the temperature upsurged in the summer season (June, July, August, and September), termite infestation was recorded high (Table 4).
The correlation of each subterranean was not strong and significant with humidity. However, the temperature and rainfall showed a significant and positive correlation (Table 4). Higher termite O. obesus and lower termite C. heimi were most abundant in September when post-monsoon occurs in Lahore.
Table 4. The correlation between climatic factors (temperature, relative humidity, and rainfall) and abundance of each termite species (O. obesus, M. obesi, C. heimi and H. indicola).
Climatic Factors
|
O. obesus
|
H. indicola
|
C. heimi
|
M. obesi
|
Temperature (°C)
|
r = 0.7002; P = 0.014
|
r = 0.5834; P = 0.053
|
r = 0.6934; P =0.015
|
r = 0.5739; P = 0.021
|
Rainfall (mm)
|
r = 0.5491; P = 0.051
|
r = 0.4998; P = 0.068
|
r = 0.6670; P = 0.026
|
r = 0.5209; P = 0.050
|
Humidity (%)
|
r = 0.3371; P = 0.262
|
r = 0.3969; P = 0.183
|
r = 0.4169; P = 0.151
|
r = 0.3256; P = 0.331
|