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Biodiversity of arthropod fauna in cabbage ecosystems of Tamil Nadu
K. Senguttuvan, Assistant Professor (Agricultural Entomology), Tamil Nadu Agricultural University, Coimbatore.

Abstract : Biodiversity of arthropod fauna in cabbage ecosystem revealed 2866 arthropods from 26 families under eight orders in sprayed and unsprayed condition. Diamondback moth, Plutella xylostella (Linnaeus), two species of aphids viz., Myzus persicae (Sulzer) and Brevicoryne brassicae (Linnaeus), cabbage whitefly Aleyrodes proletella (Linnaeus) were found to be a major pests of cabbage plants in this region. Minor pests are recorded as follows Cabbage looper, Trichoplusia ni (Hubner), Leaf roller, Sylepta lunalis (Guenee), Marmalade hoverfly, Episyrphus balteatus (de Geer), Painted bug, Bagrada picta (Fabricius) and Mealybug, Coccidohystrix insolita (Green). Natural enemies, predators of aphid viz., syrphids flies, coccinellid beetles, and spiders were recorded in this cabbage ecosystem. Larval parasitoids Cotesia plutellae of cabbage diamondback moth was recorded. Presence of mantids and hymenopterans (braconids) indicated the relative safety of the insecticides in these ecosystems. The biodiversity indices in the sprayed and unsprayed fields showed higher diversity in unsprayed fields revealing the influence of insecticidal spraying. Insecticidal usage should be carefully considered, keeping in mind the diversified insect fauna in the cabbage and cauliflower ecosystems. Observation of certain taxa to chemical sprays could contribute in the identification of bioindicators for environmental stress due to pesticide usage in the cabbage field.

Introduction: Cabbage (Brassica oleracea var. capitata L.) and cauliflower (Brassica oleracea var. botrytis L.) are important vegetables of cole crop group and the third major vegetable group primarily grown in the winter season in plains. The major cabbage and cauliflower growing states in India are Assam, Bihar, Karnataka, Madhya Pradesh, Maharashtra, Orissa, Tamil Nadu, Uttar Pradesh and West Bengal. In India, Cole crops were grown over an area of three million hectares with an annual production of 79.49 million tonnes in 2011-2012. Review of Literature Ludwig and Reynolds (1988) reported that Shannon-Weiner index (H) and Evenness index (EI) were the most widely used indices by various ecologists. They also reported that diversity indices incorporate both species richness and evenness into a single value. Diadegma semiclausum and C. plutellae were the major parasitoids of P. xylostella in cabbage ecosystem. A negative relationship existed between parasitism by C. plutellae and D. semiclausum indicating a competitive displacement between the two species (Talekar and Yang, 1993). The extent of natural parasitism of P. xylostella by these parasitoids vary between 16 and 75 per cent in tropics and 80 per cent in hilly areas (Regupathy, 1996). Larval and pupal parasitisation of DBM to the extent of 10.8 - 26.8 per cent was noticed in cauliflower ecosystem (Sable et al., 2008). The parasitisation rates of C. plutellae on DBM was to the tune of 16-50 per cent and there was a density dependent relationship between the parasitoid and the host (Jayarathnam, 1977). Mushtaque and Mohyuddin (1987) have observed decreased parasitism of DBM by C. plutellae in Pakistan during heavy use of insecticides. Studies by Talekar (1990) proved the toxicity of teflubenzuron to the pupae of D. semiclausum, the parasitoid of DBM. Class Insecta has always been regarded as the most speciose class in the Animal Kingdom (Ehrlich and Wilson, 1991; Samways, 1993; Myers et al., 2000). This class also constitutes a substantial proportion of terrestrial species richness and biomass and plays a significant role in ecosystem functioning (McGeoch, 1998). Even so, known species diversity is only a small fraction of the total species diversity (Ehrlich and Wilson, 1991; Myers et al., 2000). The performance and effectiveness of natural enemies might also be enhanced by chemical cues from the associated plants (Altieri et al., 1981; Nordlund et al., 1988). Spiders are the most abundant predators of insects in terrestrial ecosystems (Vanhook, 1971; Moulder and Reichle, 1972; Schaefer, 1974; Edwards et al., 1976) and form one of the most ubiquitous groups of predaceous organism in the animal kingdom (over 30,000 species) (Riechert and Lockley, 1984). Pesticide impact on arthropod diversity Hakim et al. (2011) found that the activities of natural enemies (predators and parasitoids) were found to be maximum in control plot followed by neem oil, imidacloprid and profenophos indicating that neem oil (repellent) was the least toxic against natural enemies followed by imidacloprid. Amalin et al. (2009) reported that more individuals of the order Orthoptera were collected in the non-sprayed area than the sprayed area, especially from the second sampling period during February for families Acrididae and Gryllidae. Studies of Rishikumar et al. (2012) revealed that the population of predators was significantly less disrupted by the stem application method, while foliar sprays were particularly destructive to beneficial pests. Agricultural field that were frequently subjected to pesticides often had lower spider populations (Amalin et al., 2001). A decrease in spider population as a result of pesticide use could result in an outbreak of pest populations (Holland et al., 2000; Tanaka et al., 2000). Riechert and Lockely (1984) reported that a spider may kill as many as 50 times the number of prey it consumes. In agroecosystems, spiders, as generalist predators, might maintain populations in periods of low pest numbers by preying upon other insects, including harmless and beneficial insects (Nyffeler et al., 1994). Materials and Methods Studies were conducted to evaluate the arthropod diversity in cabbage ecosystem during 2012 – 2013 at Jahirnayakanpalayam, Coimbatore and Erisibetta, Kotagiri and TNAU Farm, Najanadu, Horticultural Research Station, Ooty. The various methodologies followed for survey and collection of arthropods, preservation and their identification and diversity analysis are described in detail hereunder. To develop a package of methods for quantitative sampling of arthropod communities, collections were made using four different methods viz., active searching, net sweeping, pitfall trap and rubbish trap. For carrying out arthropod collection, the plot was divided into 100 quadrats (10 m x 10 m). Five such quadrats were chosen each at random and the entire plot was covered during the sampling period. Active searching was done in the early morning and evening hours. Each quadrat was selected at random and they were actively searched for arthropods. Each site was searched for a total of two hours. Spiders were collected by walking diagonally in the fields and care was taken to capture them without injuring and transferred to polythene bags for further studies. Specimens from a single quadrat at each habitat type were pooled for analysis. Sweeping is very effective for the collection of flying and jumping arthropods at the ground level and under storey vegetation. The nets used in systematic sweeping of the ground level were made of thick cotton cloth with a diameter of 30 cm at the mouth and a bag length of 60 cm. 	For carrying out net sweeps, the plot was divided into 100 quadrats, measuring 10 m x 10 m each. Five such quadrats representing the field were chosen at random and the entire ground level vegetation in the chosen quadrat was covered during the sweeping. Net sweeps were always done between 10 am and 12 noon. The arthropods collected from each quadrat were transferred to polythene bags containing cotton dipped in chloroform. Sampling was done from April 2012 to June 2012. The sweeps were made at ground vegetation above one feet height from the ground for collecting insects from plants. The contents from the sweep nets were placed in a bucket with a small amount of ethyl acetate to kill all the arthropods. They were sorted on the same day. Spiders and other arthropods were separated from the vegetation. Soft bodied insects and spiders were later separated from the bag and preserved in vials containing 70 per cent alcohol. This method was adopted to collect ground dwelling and nocturnal arthropods. Pitfall traps were set out using a plastic container (15 cm height and 10 cm width) buried in to the soil to a depth of 20 cm. Five pitfall traps were placed in each of five randomly chosen 10 m x 10 m quadrats. The traps were set up between 6 AM and 5 PM and specimens were collected the next morning. In order to stop the receptacle from filling with water or leaf litter and to deter some larger predators like mice, the trap was covered with a flat stone supported by four smaller stones. Teepol (2-3 drops) in water was kept in the traps as trapping fluid. The traps were placed at the rate of 25 per plot. The trapping fluid was changed every week. Observations were recorded daily on the number and type of arthropods trapped in each container. The collection of arthropods for biodiversity analysis was carried out in cabbage field at different stages of the crop growth. Arthropod fauna were collected fortnightly from first fortnight of April 2012 to the last fortnight of June 2012 using the methods specified earlier. The collected arthropods were sorted out based on taxon. Soft bodied insects and spider species were preserved in 70 per cent ethyl alcohol in glass vials. Other arthropods were card mounted or pinned. The preserved specimens were photographed and identified based on the taxonomic characters. All arthropod species were identified to the lowest possible taxon. Insects were identified with the help of Dr. M. Ganesh Kumar, Professor, Department of Agricultural Entomology, Tamil Nadu Agricultural University, Coimbatore and also following Lefroy (1984), Richards and Davis (1983), Poorani (2002) and Firake et al. (2012) after comparing with the specimens available in the Department of Agricultural Entomology, Tamil Nadu Agricultural University. Diversity analysis of arthropods in cabbage ecosystem Alpha diversity indices The following indices were used to assess and compare the diversity and distribution of arthropods in cabbage ecosystem. Species richness and diversity version ii (Pisces Conservation Ltd., www.irchouse. demon.co.uk) (Henderson, 2003) programmes were used to assess and compare the diversity of arthropods in sprayed and unsprayed cabbage ecosystems. Species richness Fishers alpha (Fisher et al., 1943) This presents the alpha log series parameter for each sample. This is a parametric index of diversity that assumes the abundance of species following the log series distribution. αx,〖αx〗^2/2,〖αx〗^3/3,〖αx〗^n/n Where, each term gives the number of species predicted to have 1, 2, 3, … n individuals in the sample. Q Statistic (Kempton and Taylor, 1976) This presents the interquartile diversity index for each sample. It measures the interquartile slope of the cumulative abundance curve and is estimated by, Q=1/2 nR_1+∑▒nr+(1/2 nR_2)/ln⁡(R_2/R_1 ) where, nr - the total number of species with abundance R R_1 and R_2 – 25 per cent and 75per cent quartile of the cumulative species curve nR_1 - the number of individuals in the class where R1 falls nR_2 - the number of individuals in the class where R2 falls Species number (Magurran, 1987) This represents the total number of species in each sample. Margalef’s D (Clifford and Stephenson, 1975) Margalef’s D has been a favourite index for many years. It is calculated as species number minus one divided by the logarithm of the total number of individuals. This program uses the natural logarithm. D_Mg=((S-1))/ln⁡N where, S - total number of species recorded N - the total number of individuals summed overall S species Shannon diversity index (Batten, 1976) This represents the Shannon - Weiner (also called as Weaver) diversity index for each sample and is defined as: H^'=∑▒〖P_i ln⁡〖P_i 〗 〗 where P_i - The proportion of individuals in the ith species H^' - This program calculates the index using the natural logarithm Brillouin diversity index (Magurran, 1987) The Brillouin index H is calculated as follows: H=ln⁡N!-∑_(i=1)^s▒ln⁡〖n_i !〗/N where, N - is the total number of individuals in the sample n_i - is the number of individuals belonging to the ith species and s is the species number. Species Dominance indices Simpson’s index (Simpson, 1949) Simpson’s index describes the probability that a second individual drawn from a population should be of the same species as the first. D=∑▒[N_i (N_i-1) ]/[N_t (N_t-1) ] where, N_i - is the number of individuals in the ith species N_t - is the total number of individuals in the sample So, larger its value, greater the diversity. The statistic 1 - C gives a measure of the probability of the next encounter being from another species (Hulbert, 1971). Berger Parker diversity index (Berger and Parker, 1970) A simple dominance measure is the Berger Parker index. The index expresses the proportional importance of the most abundant species. d=N_max/N where, N_max -	is the number of individuals in the most abundant species N - is the number of individuals in the sample This simple index was considered by Batten (1976) to be one of the best. It is simple measure of the numerical importance of the most abundant species. McIntosh index (McIntosh, 1967) This index was calculated using the following formula proposed by McIntosh (1967) as D=(N-U)/(N-√N) where, N 	is the total number of individuals in the sample U 	is given by the expression, U=√(∑▒n_i^2 ) Where, n_iis the number of individuals belonging to the ith species and the summation is undertaken for over all the species. Evenness indices Evenness (E) is a measure of how similar the abundances of different species or categories are in a community. When all species in a community are equally abundant, the evenness index should be maximum and decrease towards zero as the relative abundances of the species diverge away from evenness closer to zero. It indicates that most of the individuals belong to one or a few species or categories, when the evenness is close to one; it indicates that each species / category consists of the same number of individuals. E=H'/ln⁡〖(S)〗 where, S – Total number of species in a community H’ - prime is the number derived from the Shannon diversity index Equitability (Magurran, 1987) Equitability or evenness refers to the pattern of distribution of the individuals between the species. This measure of equitability (J) compares the observed Shannon- Weiner index against the distribution of individuals between the observed species which would maximize diversity. If H is the observed Shannon - Weiner index, the maximum value this could take log⁡S, where S is the total number of the species in the habitat. Therefore the index is: J= H/log⁡S Results Collection and identification of arthropods under cabbage ecosystem Arthropods collected at fortnightly intervals from April to June (2012) in sprayed and unsprayed cabbage fields were documented, identified up to the  lowest taxonomic level possible and various biodiversity indices were worked out. The survey yielded a wide array of 2866 individuals of arthropods from 26 families and eight orders of insects (Tables 1). The class Insecta was the most common followed by Arachnida. Totally, six families of Lepidoptera were collected with the majority of individuals falling under the family Plutellidae and Pyralidae in both sprayed and unsprayed cabbage fields. Among the endopterygotes, maximum individuals were from Lepidoptera, while Hemiptera was predominant in terms of individuals of exopterygota. Among the four families of hemipterans collected, majority of the individuals were from Aphididae and Pentatomidae followed by Pseudococcidae (Table 1). In case of Aphididae, 310 individuals of Myzus persicae (Sulzer) were collected with majority of individuals from unsprayed cabbage. Orthoptera was represented by three families viz., Gryllidae (Gryllus sp.), Pyrgomorphidae (Chrotogonus sp.) and Tettigoniidae (Conocephalus sp.) with majority of individuals from unsprayed cabbage field. The single family represented under the order Mantodea was Mantidae with 16 individuals of Mantis religiosa Linnaeus from unsprayed field. The order Hymenoptera was represented by four families. The maximum number of individuals belonged to family Braconidae (249), followed by Ichneumonidae (74) and Tenthredinidae (44) in both sprayed and unsprayed cabbage. Diptera was represented by three families with majority of individuals collected falling under Syrphidae of all genus (143) followed by Tachnidae (103) and Tipulidae (31). Majority of species under Tachinidae belonged to the genus Exorista larvarum Linnaeus (64). Under Coleoptera three families were collected with majority of individuals belonging to Coccinellidae (110). Only 27 individuals of Meloidae were collected (Table 1). Biodiversity indices From the collection, 8 orders of arthropods were recorded (Plates: 1 - 6). Based on this primary arthropod data, different sets of alpha diversity indices were calculated. Alpha diversity indices at ordinal, family, generic and species level The species number calculated based on the generic level varied between a minimum of 32 during the first fortnight of April to a maximum of 40 during second fortnight of June in unsprayed cabbage. In sprayed cabbage, the maximum (38) was during the first fortnight of May and the minimum (26) during the first fortnight of April (Table 2). Based on ordinal level and species level analysis, the species richness was not clear in variation from the Fisher’s alpha index values. At generic level, the value was the highest in the first fortnight of May in sprayed field (10.198). The highest ordinal and familial level indices were 1.8397 in first fortnight of June and 7.8919 in second fortnight of June in sprayed cabbage (Table 3). From Table 4 it could be seen that the Margelef’s D value based on generic level varied between a minimum of 4.5213 during the first fortnight of April and maximum of 6.1451 during first fortnight of May in sprayed cabbage. In unsprayed cabbage, the index value was the highest during the second fortnight of June (6.6195) and the lowest during the first fortnight of April (5.9322). Analysis of data using Q statistic is presented in Table 5. The index value based on ordinal level ranged from 1.5922 to 3.1423 and 1.4923 to 1.8766 in sprayed and unsprayed cabbage fields, respectively and showed significant variation. On the generic level, the value was maximum in the first fortnight of May (6.1451) and minimum in the first fortnight of April (4.5213) in sprayed cabbage. In unsprayed cabbage, the value was the highest in the first fortnight of May (20.025) and the lowest in the first fortnight of June (13.395). Minimum variation was observed in case of Brillouin diversity index based on ordinal, generic, familial and species level between the sprayed and unsprayed cabbage (Table 6). The Shannon –Weiner index was calculated based on the four taxonomic levels and presented in Table 7. The index values based on ordinal, generic, familial and species levels in sprayed cabbage were lower than unsprayed field. Simpson’s diversity indices at ordinal, family, generic and species level The Simpson’s index calculated based on ordinal level revealed maximum during the second fortnight of June (4.3064) and minimum during the second fortnight of April (3.5229) in unsprayed cabbage. In sprayed cabbage, the maximum was during the second fortnight of June (5.1852) and minimum during the first fortnight of April (3.1437). Analysis of values based on generic level showed that the value was the highest during the first fortnight of April and lowest during the second fortnight of April both in unsprayed cabbage field (Table 8). McIntosh index also showed no clear variation among the values on the four taxonomic levels in both sprayed and unsprayed cabbage (Table 9). Berger Parker diversity index was calculated based on the four taxonomic levels. The index value was higher in unsprayed cabbage than sprayed field and no variation in generic level and species level in sprayed and unsprayed field, respectively (Table 10). Evenness indices (Equitability J) also observed clear variation in the values of Familial level the maximum (0.83015) was noticed on second fort night of June in sprayed field but in the unsprayed field noticed maximum (0.82426) at first fortnight of April (Table 11). The maximum number of arthropods was observed in unsprayed cabbage than sprayed field. The maximum diversity of arthropods occurred in the month of May with most of the diversity indices. Discussion Comparison of abundance and diversity of arthropods in cabbage ecosystem Arthropods are frequently used as ecological indicators because they represent more than 80 per cent of the global species richness. They fulfil essential roles in ecosystem such as pollination, soil structure and function, decomposition and nutrient recycling, natural enemies of pest species, prey for highly valued vertebrate, etc., (Pettersson et al., 1995). They have short generation times and respond quickly to ecological changes. Further, various arthropod taxa have been used to detect anthropogenic impact on ecosystems including agriculture and climate change (Parmesan, 1996; Buddle et al., 2000). The results of the present study revealed that arthropod diversity was greater in case of unsprayed cabbage compared to sprayed cabbage field. Biodiversity is a measurement of ecological complexity, and is expected to be higher in less disturbed ecosystems; overall, biodiversity is highly threatened by modern agriculture documented by Amman (2005). The most significant decline in arthropod density was found in the rice fields where broad-spectrum insecticides were applied as noticed by Yun (1997). Agricultural intensification through use of pesticides is significantly correlated to reduction in various taxonomic levels. Arthropod diversity in agricultural landscapes was found to be higher in less intensely cultivated habitats as observed by Amman (2005). Biodiversity of arthropod fauna assessed in brassicaceous ecosystems by Firake et al. (2012) Three species of aphids viz., Lipaphis erysimi Kaltenbach, Brevicoryne brassicae Linnaeus and Myzus persicae Sulzer, and large white cabbage butterfly (Pieris brassicae Linnaeus) as major pests of brassicaceous plants in Meghalaya region. The present investigation yielded 2866 individuals of arthropods belonging to 26 families and eight orders in both sprayed and unsprayed cabbage fields. Under Insecta, endopterygotes were the largest group represented by four orders, while exopterygotes represented by three orders. Among endopterygotes, maximum individuals were from Lepidoptera while Hemiptera was predominant in terms of individuals of exopterygota. Totally, six families of Lepidoptera were collected with the majority of individuals falling under the family Plutellidae and Pyralidae in both sprayed and unsprayed cabbage fields. The four families of hemipterans were collected and the majority of the individuals were from Aphididae and Pentatomidae followed by Pseudococcidae. Amoung Aphididae, with majority individuals of Myzus persicae Sulzer were collected from unsprayed cabbage. Orthoptera was represented by three families viz., Gryllidae, Pyrgomorphidae and Tettigoniidae with majority of individuals from unsprayed cabbage field. The single family represented under the order Mantodea was Mantidae with major individuals of Mantis religiosa Linnaeus from unsprayed field. The order Hymenoptera was represented by four families. The maximum number of individuals belonged to family Braconidae, followed by Ichneumonidae, Tenthredinidae and Apidae in both sprayed and unsprayed cabbage. Studies on diversity and abundance of DBM parasitoids in Thailand revealed that C. plutellae was dominant during early crop stages as reported by Haseeb et al. (2005) and Upanisakorn et al. (2011). Diptera was represented by three families with majority of individuals collected falling under Syrphidae followed by Tachnidae and Tipulidae. Majority of species under Tachinidae belonged to the genus Exorista. Under Coleoptera three families were collected with majority of individuals belonging to Coccinellidae. Only 27 individuals of Curculionidae were collected. Earlier studies with spiders of the family Oxyopidae susceptible to insecticides such as the pyrethroid alphamethrin, but less so than to other insecticides such as endosulfan was reported by Vandenberg et al. (1990). Spiders were particularly susceptible to organo-synthetic insecticides such as carbamates and organophosphates, while fungicides, herbicides, and natural insecticides such as Bt had little or no toxicity for spiders as documented by Stark et al. (1995). Biodiversity indices Biodiversity is a function of species present (species richness), the evenness which individuals (Fig. 26) are distributed among these species (species evenness) and the interaction component of richness and evenness as documented by Ludwig and Reynolds (1988). Measures of diversity are frequently seen as indicators of the well being of any ecosystem. They also serve as a measure of the species diversity in the ecosystem. As complete counts of organisms are impractical, indirect solutions that are practical, rapid and inexpensive are necessary and hence, diversity indices have gained importance. In the present study, the data on the arthropods collected were subjected to alpha or within habitat diversity and beta or between habitat diversity of sprayed and unsprayed cabbage fields. Margelef’s D value based on generic level varied between a minimum of 4.5213 during the first fortnight of April and maximum of 6.1451 during first fortnight of May in sprayed cabbage. In unsprayed cabbage, the index value was the highest during the second fortnight of June (6.6195) and the lowest during the first fortnight of April (5.9322). Similar results were earlier reported by Stanley (2007) that the overall species richness indicated by Margelef index was 2.60 for sprayed and 2.03 for unsprayed clumps for eight sprays of diafenthiuron at 0.08 per cent. In current study, alpha diversity was estimated based on species number, Fishers alpha index (Fig. 27), Margelef’s D index (Fig. 28), Q statistic (Fig. 29), Brillouin index (Fig. 30) and Shannon-Weiner index (Fig. 31) while dominance was based on Simpson’s index, McIntosh index and Berger parker index. In both instances, the analysis was subjected to four levels of classification viz., based on order, family, genus and species. The use of higher taxa typically families as surrogate for species has been suggested by Williams and Gaston (1994). Hughes (1978) concluded that the taxonomic level of identification is one of the most important factors influencing the value of the Shannon index. The species richness indices based on species number, Fishers Alpha index, Margalef’s D index, Q Stastistic, Brillouin diversity index and Shannon - Weiner index was higher in unsprayed cabbage. The different dominance indices viz., Simpson’s index (Fig. 32), McIntosh index (Fig. 33) and Berger Parker index (Fig. 34), expressed higher arthropods diversity in unsprayed cabbage field and lower was observed in sprayed field. The present study was supported by Stanley (2007) who reported that diafenthiuron did not have any adverse effect on the pest, pollinator and natural enemy diversity which was measured by using indices of species richness, diversity and evenness (Fig. 35). His study also supported the all species richness indicated by Menhinick index (1.77 and 0.93) and Simpson’s index of diversity (0.17 and 0.28) in sprayed and unsprayed fields, respectively. However, survival comes to normal state at 21 days after the next spray (second spray). This was evidenced by the same Simpson’s index of 0.26 and 0.20 in the sprayed and unsprayed area, respectively. The current biodiversity study demonstrated that the chemicals applied in the sprayed area had a negative effect on the arthropod community as a whole. The current findings on the sensitivity of certain taxa to chemical sprays could contribute in the identification of bioindicators for environmental stress due to pesticide usage in the cabbage field. Therefore, the use of the best management practices should be taken into serious consideration in controlling the pests in the agricultural areas to reduce the negative impacts on biodiversity and continuously provide natural ecological services such as biological control.

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