Diversity of Spiders (Arachnida: Araneae) Recorded in Khasi Mandarin Ecosystem of Northeastern India

Citrus is the third most important fruit crop of India, grown over an area of about 10.39 lakh ha with an annual production of 13.18 million tonnes (National Horticultral Board, 2019). Among the various species of Citrus, Khasi Mandarin (Citrus reticulata Blanco) is the most popular and economically important cultivar of North East India which is historically believed to be the centre for the dissemination of Citrus to other parts of the world (Srivastava and Singh, 2006). In India, Khasi Mandarin constitutes about 43.6% of the total Citrus fruits production, covering nearly 38.2% of the total Citrus cultivation area (Tariang et al., 2018). Khasi Mandarin occupies the major area in the northeastern India due to its high commercial importance in with respect to its production and export value (Deshmukh et al., 2016). In the North East Region (NER), Assam is the leading producer of Khasi Mandarin with a production of 598.96 thousand tones, covering an area of 105.49 thousand hectares of total 0.31 million hectares (Sangma et al., 2018). Khasi Mandarin is known for its flavour, juice content and superior soluble sugar and acidity ratio (Deka et al., 2018). Given its position as one of the major commercial crops of Northeastern region, an increase in the infestation of Citrus orchards by insect and arthropod pests has led to the incurrence of huge annual losses and yield reduction (Kakoti et al., 2019). Severe incidence of pests viz. Trunk borer (4.40 to 48.65%), Bark eating caterpillar (10.80-43.76%), citrus leaf miner (4.00 to 49.27%) and Citrus butterfly (3.32 to 27.89%) have been reported by Deka et al., 2016. Extensive use of pesticides to manage pest complexes in orchards has resulted in secondary pest emergence, development of pesticide resistance and loss of biodiversity among others. The growing concern over the harmful residual effects of pesticides on the environment and human health demands for the urgent need to look for innovative biological pest management practices. One of the most efficient and self sustainable bio control agents are natural enemies of the pest species in the form of predators or parasitoids.
       
Spiders (Class Arachnida: Order Aranae) are generally recognized as one of the most varied and functionally important invertebrates (Basumatary and Brahma, 2017). There are approximately 49669 species of spiders belonging to 4228 genera and 129 families worldwide (World Spider Catalogue version 21). In India, a total of 1686 species belonging to 60 families and 438 genera have been reported till date (Keswani et al., 2012). By virtue of their polyphagous nature, spiders play an important role in regulating the arthropod population in various agro-ecosystems (Sunderland, 1999). Spiders are recognized as dominant insectivores in many agro-ecosystems due to their predatory behaviour. Spiders have been used successfully against various Citrus pests under both laboratory and field conditions (Xiao et al., 2007). Considering the rich faunal diversity of spiders in Northeastern India and their role as efficient natural predators, an attempt was made to document and study the diversity of different spider species in the Khasi Mandarin Ecosystem of the Northeastern parts of India.

The northeastern region of India lies at the conjugation of Indo-Himalayan mega biodiversity hotspot. The region lies at 21^o50' and 29^o34'N latitude and 85^o34' and 97^o50'E longitude. Field observations were carried out during a period of five years, from May 2016 to May 2021 in the North Eastern states of Assam (Kamrup, Jorhat, Goalpara, Karbi Anglong, Dibrugarh and Tinsukia districts), Arunachal Pradesh (Lohit, Lower Dibang Valley and East Siang districts), Nagaland (Dimapur district), Manipur (Tamenglong, Bishnupur and Noney districts), Meghalaya (Ri-Bhoi and West Garo Hills districts), Mizoram (Kolasib, Lunglei and Aizawl districts) and Tripura (Sipahijala and Gomati districts). The spiders were collected quarterly at an interval of 3 months from Citrus reticulata orchards using methods suggested by Tikader (1987). The sampling was conducted randomly from four different sides of the lower branches of the plant. The spiders resting on the orb webs or plant parts were collected by placing a jar containing spirit below the spider and slightly tapping the spider into it. The collections were either made in the early hours of the mornings or in the evenings as the spiders are less active during these times. The spiders collected during each sampling were brought to laboratory, washed with alcohol, stored in a mixture of 75% ethyl alcohol with proper labeling of locality, date of collection and name of the host plant along with other notes of importance. The preserved spiders were later examined under stereomicroscope Labomed CZM6 in the laboratory and identified with the help of taxonomic keys and available literature. On the basis of the rate of occurrence, the spiders were divided into four categories viz. very common (spiders found in >35 collections), common (15<35 collections), rare (5<15 collections) and very rare (<5 collections) (Bhat et al., 2013).

During the course of the study, individuals belonging to 19 species, 16 genus and 8 different families were recorded. The observed data (Table 1) indicates that the most abundant species belonged to the family salticidae (36.84%) followed by the family araneidae (26.31%). The family oxyopidae (10.52%) ranked third with respect to diversity of species. The five families hersiliidae, heteropodidae, pisauridae, tetragnathidae and thomisidae had the lowest amount of species diversity at 5.2% each. Based on the classification given by Uetz et al., (1999), the spider population belonged to four different foraging guilds as illustrated in Fig 1. Stalkers were the most abundant group at 47.37%, followed by orb-weaver population of 31.58% while foliage runners and ambushers were found in equal amounts at 10.53% each. The spider species observed in the Khasi Mandarin Ecosystem are given in Fig 2.   
 

 

 
                      
       
Although the maximum population of spiders was observed during the winter months, there were considerable exceptions with respect to the individual families as well as species. In general, the spiders were found throughout the year but the least amount of population was recorded during the peak summer months. Individuals belonging to the family Salticidae were recorded throughout the year with a negligible amount of fluctuation. Among the individuals of the family Salticidae, the highest recorded species was Telamonia elegans followed by Carrhotus spp. Individuals belonging to the Carrhotus decorata, Telamonia dimidata and Hasarius spp. were also recorded, though in smaller amounts, showing their considerable presence in the ecosystem. The members of the family Araneidae ranked second highest in species diversity. The highest population belonged to the Araneus spp. The second highest population was recorded for the Neoscona spp. which was usually found active after sunset. Also, the occurrence of Neoscona spp. coincided with the onset of rainy season. Eriovixia spp., Eriovixia laglaizei and Thelacantha brevispina were also recorded from the orchards. In case of the family Oxyopidae, the dominant species was Oxyopes birmanicus though a considerable population of Oxyopes shweta was also recorded. The members of the family Oxyopidae were observed in relatively large numbers during late August and early September. Although the two families Tetragnathidae and Hersiliidae lacked any species diversity, the populations of the individual species were in relatively large numbers. Overall, the highest population of individuals was recorded for Oxyopes birmanicus followed by Telamonia elegans with Carrhotus spp. and Tylorida spp. having the third and fourth highest populations, respectively. The lowest population belonged to Neoscona spp.
       
The Northeastern hilly region of India has a diverse population of spiders but much of it still remains unexplored. A few surveys have tried to document the spider diversity of North East India (Biswas and Majumder, 2006; Biswas and Majumder, 2007; Anindita et al., 2017) but it falls short considering the status of north-east India as a biodiversity hotspot. The results obtained during the present study confirm the presence of a complex and rich community of spiders in the Khasi Mandarin ecosystem of Northeastern India. The species diversity and distribution of spiders often vary from one geographical area to another due to slight changes in the habitat structure, complexity and microclimate (Downie et al., 1999). High species diversity allows more healthier and complex interactions among the members of the community and is hence considered an indicator of good environmental conditions (Hill, 1973).
       
Citrus orchards have long since offered a semi permanent habitat harboring a rich and abundant arthropod fauna that enables more self-sustained spider populations to exist (Monzo et al., 2011). Alvis (2003) reported the occurrence of 55 spider species in the Citrus canopy of a Citrus-growing area. Over the years, spiders have been used as biocontrol agents of many Citurs pests in different parts of the world. A population of spiders, dominated by Chiracanthium mildei played a prominent role in the management of scale Ceroplastes floridensis in the commercial Citrus groves of Northern Israel (Mansour and Whitecomb, 1986). In Florida, the three species of sac spiders, Chiracanthium inclusum, Hibana velox and Trachelas volutus, were reported as important predators of citrus leaf miner, Phyllocnistis citrella (Amalin et al., 2001).
       
Apart from a few exceptions, the trend in species diversity was more or less the same all throughout the entire northeastern region. The most abundant species belonged to the families Salticidae and Araneidae in all the Khasi Mandarin cultivation areas. Salticidae and Araneidae have displayed high species richness and are more often than not found to be the predominant families in many ecosystems. Sudhikumar et al., (2005) recorded the highest number of species (17) of Salticidae belonging to 15 genera in the rice agroecosystem of Kerala. Among 21 families of spiders, captured from the Punjab province of Pakistan, Salticidae was the prominent family (31.09%) with 9 genera and 27 species (Parveen et al., 2007). During the study of the occurrence of spiders in major fruit crops of Punjab, highest genetic diversity was observed in Salticidae, followed by Araneidae and Oxyopidae (Singh et al., 2020). In the Wayanad plateau of Western Ghats, Araneidae was the dominant family constituting 24 species from 10 genera (Jose, 2010). Araneidae was also found significantly (28.14%) in Barpeta district of Assam, whereas the spider family Hersilidae had the least population (Singh et al., 2012). Chetia and Kalita (2012) found the distribution of some families (Araenidae, Aalticidae, Tetragnathidae) to be continuous.
       
During the present study, most of the spider species found in the Citrus ecosystem were recorded all throughout the year. In general, a rise in the number of spiders was first observed during the early month of March, with the population attaining a peak during August-September. Most of the population tended to decline during late December-January. Similar to the results obtained during the current investigation, Tahir et al., (2011) reported abundance of adult spiders during the month of August in the citrus orchards of Lahore, Pakistan. Tahir et al., (2015) observed that there was a strong positive correlation between abundance of insect pests and spiders (predators) which suggested that spiders could effectively control insect pest populations in the field. This conclusion is concurrent with the findings of the present investigation as the peak rise in population of spider coincided with that of the peak period of infestation by citrus pests.

The observations made during the present investigation hopes to serve as a preliminary study on the spider diversity found in the Khasi Mandarin orchards of North-East India. Spiders play an important role in the ecosystem and exploiting their role as in pest management strategies cannot take place if the species involved are not known. Going forward, extensive studies should be carried out to record the species diversity to grasp a more in-depth knowledge of the predator-prey interactions between spiders and citrus pests. The various factors influencing the faunal diversity of the area need to be investigated as well.