ISSN No. 0974-6234

Environmental Information System

Theme : Ecosystem Services ENVIS Centre on Faunal Diversity Vol. No. 23 Issue No. 3 March, 2017

Editor-in-Chief From the Director’s Desk Dr. Kailash Chandra, Director, ZSI The benefits humans receive from nature are manifold, and are defined as Associate Editor Dr. K. C. Gopi, Scientist-F ecosystem services. These services categorized as provisioning, regulating,

Editorial Board cultural and supporting are so crucial that their decline will impose a serious Dr. Rajmohana K., Scientist-D threat to the very survival of mankind. The food we eat and the water we drink (Coordinator ENVIS) are all provisioned by our ecosystems. Only a healthy ecosystem can deliver these Dr. L. K. Singh, Scientist-D Dr. Sheela S., Scientist-D services and truly speaking biodiversity underpins these ecosystem services. Most

ENVIS TEAM of our agricultural crops are pollinated by , especially bees. The recent decline in the wild bee Dr. Rajmohana K. population, is an issue of great concern, since it can hamper the global food production. Factors like Scientist-D, Coordinator habitat modification and fragmentation, degradation of landscapes, rampant use of pesticides and Shri Amitava Roy Sr. Statistical Assistant climate change are affecting our ecosystems in a large scale, resulting in a decline in their services. Shri Tridip Kr. Datta The concept, 'economics of ecosystem services' has been launched to make visible these services in Programme Officer decision making, through structured valuation in economic terms. Shri Mridul Purakayastha IT Assistant (Data Entry) MoEF & CC, is to set up Long Term Ecological Observatories (LTEO) at 8 sites in India -Western Shri Bappaditya Samanta Himalayas, eastern Himalayas, north-western arid zone, central Indian forests, Western Ghats, IT Assistant Andaman & Nicobar Islands, Jammu & Kashmir and Sundarbans, in order to monitor and study how ecological systems are responding to our changing climate. Dr. Kailash Chandra Director

Necrophagous flies (Insecta: Diptera) and their role in maintaining ecosystem balance – Garima Hore & Dhriti Banerjee ...... 2 Valuing pollinators – Palatty Allesh Sinu ...... 6 Ecosystems services provided by dung – Sabu K. Thomas & Nithya Sathiyandran ...... 9 Ecosystem services of – Rasneet Lobana ...... 13 2 ENVIS Newsletter

NECROPHAGOUS FLIES (INSECTA: DIPTERA) AND THEIR ROLE IN MAINTAINING ECOSYSTEM BALANCE Garima Hore1 *and Dhriti Banerjee2 Diptera Section, Zoological Survey of India. Email: [email protected] , [email protected] *Corresponding author

INTRODUCTION Necrophagy is the act of feeding on dead or decaying flesh. Though scavenger vertebrates, like vultures and jackals, form an important part of the detrivore community by feeding on the dead organism, the role played by the necrophagous is also of immense significance from ecological perspectives (Anderson 1995; Amendt et al. 2004). Detrivores influence the decomposition of detrital resources in virtually all natural systems, with broad consequences for community structure and ecosystem function (Seastedt and Crossley 1984; Moore et al. 2004). By shredding, consuming and transforming organic detritus, detrivores not only accelerate microbial decomposition but also helps in nutrient cycling (Edwards et al. 1970; Kitchell et al. 1979; Vossbrinck et al. 1979; Lussenhop 1992). Carrion is a specialised microhabitat characterized fundamentally by its rapid ecological successions, being an extremely transient micro-ecosystem that is rapidly degraded by the action of the arthropods that colonize them. It represents not only a rich source of energy, but also a very specialized habitat that is exploited, in most cases, by very specific entomological fauna. The arthropods involved in succession vary according to geographical areas, even in places with similar climates. Also, the number of individuals and the species colonizing these microhabitats vary enormously from one patch to another, and also through time (Galante and Marcos-Garcia 2004). Necrophagous insects, often called carrion insects, are key players in the decomposition process which is associated with decaying human and animal remains and utilized by insects as their micro-niches, thus, forming diverse micro-communities (Allee et al. 1949; Kuusela and Hanski 1982). A diverse fauna of necrophagous species that form this important community belong to the groups viz. Coleoptera, Diptera, and Arachnida (Amendt et al. 2000; Amendt et al. 2004; Gruner et al. 2007). A variety of necrophagous insect species occurs on or around a cadaver and, depending on their preference for a given stage of decomposition, a certain chronological sequence of colonization is supposed to take place (Byrd and Castner 2010). The groups of arthropods involved in the processes of decomposition of animal and remains belong to many taxa, but the first wave of colonization of dead and are the true flies. Necrophagous flies belonging to insect order Diptera are the initial and often the most important consumers of carrion and play a significant ecological role as decomposers by aiding in ecological processes like nutrient recycling and additionally, represent an important insect community utilised in criminal investigations as well (Catts and Goff 1992).

MATERIALS AND METHODS The present study is a brief summary of our own studies on forensic flies along with information gathered from relevant taxonomic literature (Senior-White et al. 1940; Smith 1986; Nandi 2002) and consulting a number of published research articles both from India and abroad. The images of the necrophagous flies provided are actual images obtained from forensic dipterological studies done in Kolkata by Diptera Section, ZSI.

RESULTS 1) The families of necrophagous Diptera: Sarcophagidae, Calliphoridae and Muscidae are reported as the predominant necrophagous dipteran families, known worldwide, though a number of families like phoridae, psychodidae, sepsidae, stratiomyidae, fanniidae, anthomyiidae, piophilidae, chloropidae, ephydridae, milichiidae, neriidae, micropezidae, drosophilidae, dixidae, sphaeroceridae and cecidomyiidae have also been reported to visit carcasses (Smith 1986; Song et al. 2008; Dupont et al. 2011; Dupont et al. 2012; Ndueze et al. 2013; Pereira de Sousa et al. 2014; Cavallari et al. 2015; Pereira de Sousa et al. 2015; Rochefort et al. 2015; Pereira de Sousa et al. 2016). Common necrophagous fly families recorded from India known for colonizing corpses are mostly the calliphorids, sarcophagids and muscids, visiting carcasses whereas flies from families like fannidae, stratiomyidae, phoridae, sepsidae, piophilidae, neriidae, anthomyiidae, ulidiidae have also been reported (Figure 1) (Joseph and Parui 1980; Bharti and Singh 2003; Majumdar et al. 2007; Sinha 2009; Bharti 2012; Chakraborty et al. 2013; Chakraborty et al. 2014a, 2014b; Chakraborty et al. 2015a, 2015b, 2015c; Jadav and Sathe 2015a, 2015b ; Archana et al.2016; Chakraborty et al. 2016a, 2016b; Khullar et al. 2016; Singh et al. 2016; Chakraborty et al. 2017). Vol. No. 23(3) : March, 2017 3

A B

Fig. 1: Necrophagous flies feeding on carcass of bird (A) and fish (B)

2) Ecosystem services provided by necrophagous flies: i) Decomposers which help in nutrient cycling and maintaining ecological balance: In any natural or semi-natural habitat, three types of organisms exist: producers, consumers and decomposers. Good functioning of the ecosystem will depend on their suitable action and interaction. The viability of every ecosystem is based on the normal functioning of its nutrient cycle. The activity of decomposers benefit humus formation in the soil, and the availability of nutrients for plants. The process of decomposition is one of the most important events in the functioning of ecosystems (Galante and Marcos-Garcia 2004). Despite their small sizes and cumulative biomass, necrophagous dipterans commonly have significant effects on carbon and nutrient cycling by modulating the quality and quantity of resources that enter the detrital food web, with consequences at the ecosystem level (Yang and Gratton 2014). Thus, the importance of necrophagous flies, an important section of the detrivore community is not only the ingestion of carrion, but also in making the carrion available to microorganisms. The action of the larvae of flies and other insects, for example, results in liquefaction of corpse tissues and prepare the substratum for the intervention of microbial decomposers (Galante and Marcos-Garcia 2004).This, in turn, helps in recycling of carbon and nutrients like nitrogen and phosphorus in the ecosystem, making them accessible to the producers. ii) Necrophagous flies as potential bioindicators for detecting environmental changes: The Diptera are potentially useful bio -indicators for the evaluation of impact of environmental changes and the monitoring of forest recuperation (Majer 1987). Their suitability is based on the fact that they tend to be very numerous, which facilitates the collection of large quantities of specimens, and are also taxonomically pretty diverse. This permits the analysis of community-level effects, based on the varying contribution of different species. Diptera also occupy a wide variety of niches and several different trophic levels (Majer 1987). Given their ecological diversity, dipterans, both larvae and adults can be found in a wide range of habitats, both in the wild and in anthropogenic environments in rural or urban contexts (D'Almeida and Lopes 1983). Since individual dipteran species are often restricted to a narrow range of environmental conditions, analyses of dipteran community composition can prove to be sensitive indicator faunae for detecting even subtle changes in the environment (Pereira de Sousa et al. 2014; Odat et al. 2015). Species of dipteran families like Calliphoridae and Sarcophagidae are found in both natural and anthropogenic environments. They differ substantially, however, in their sensitivity to man-made impacts. For instance, studies show that sites of intermediate impact had a higher diversity of calliphorids and sarcophagids than those, where disturbance was either intense or totally absent (Dufek et al. 2016). Similar studies carried out in India could provide the basis of considering specific necrophagous dipterans as potential bio-indicators of environmental changes. 3) Role of necrophagous flies in determining PMI- applications in forensic entomology: Knowledge of the stages of development as well as succession of insect species which takes place in a corpse following death has been used in studies of forensic entomology for estimation of the time elapsed since death. By studying the insect population and the developing larval stages, forensic scientists can estimate the post-mortem interval (PMI) which ultimately helps in determining the cause of death (Amendt et al. 2004; Joseph et al. 2011). DISCUSSION AND CONCLUSION Decaying carrion provides a transient, rapidly changing resource which supports a large, dynamic fly community thus aiding in estimation of PMI and criminal forensic investigations. Necrophagous dipterans are the initial wave of insects to colonize carcasses, 4 ENVIS Newsletter commencing the process of decomposition. Though the adults feed on the fluids of the corpse, the larvae are the true decomposer organisms, secreting enzymes directly into the carrion and helping with the liquefaction of the corpse tissues while assisting the increase of microbial activity, thus playing a crucial role in nutrient cycling and maintaining homeostasis of the ecosystem. The anthropophilic nature of sarcosaprophagous Diptera also make them, as recent research shows, ideal candidates for functioning as bio-indicators and assessing short term and long term environmental changes. 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VALUING INSECT POLLINATORS Palatty Allesh Sinu Department of Animal Science, Central University of Kerala, Riverside Transit Campus, Padannakad PO 671314, Kerala, India & Department of Ecology and Evolutionary Biology, University of Arizona, Bioscience West, 1041 E Lowell, Tucson 85721, Arizona, USA Corresponding author: [email protected]; Contact no. (+91) 8547887834

The assessment and valuing ecosystems as the natural capital is the philosophy of ecosystem services. It has been assessed to have a tremendous value, because almost everything the humanity access and use are directly or indirectly belonging to the nature. While these services have been used and often commercially exploited, the natural capital has declined dramatically. It has affected the stability of several kinds of terrestrial and aquatic ecosystems in the world. Therefore, conservation biologists use ecosystem services and functions rather than the biodiversity per se recent days to draw the attention of the policy makers for conservation of habitats and ecosystems. Unfortunately, many underdeveloped countries have used these services to market their biodiversity with very limited investment made for the conservation of species and their habitats. For instance, the wild medicinal plants were the resources of the folk medicine. Unfortunately, many multinational companies have possessed the license and the patents for commercial production that our forefathers were using in a very sustainable fashion. The commercial exploitation has affected the population structure of these plants in the wild habitats. Among services the ecosystem provide to the humanity as assessed by the Millennium Ecosystem Assessment (2005), which include oxygen, energy, water, firewood, fodder, food, medicines, and so on, pollination has an important place, because over 70% of the food crops that we depend for our nutrition are animal pollinated (Klein et al. 2007; Garibaldi et al. 2013). For the same reason, the world is perceiving pollination as a service having tremendous impact to the food security, nutrition, poverty eradication, and overall human development in underdeveloped parts of the world (Chaplin-Kramer et al. 2014; Bailes et al. 2015). There are two services the pollinators are directly extending to the peoples. First, the service of pollination in the crops and other ecologically and economically important plants and second, the bee culture and honey production. Both the services therefore support the livelihood of the forest villagers and other rural communities directly or indirectly, and the sources of foreign income to our nation. The Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) report that the honey production from the European honeybee alone is 1.6 million tons per year and the beewax production is 65,000 tons/year. In India, National Bee Board (NBB) facilitates the promotion of honey production through linking the major companies such as Dabur India with the individual farmers, self-help groups, and other kinds of firms. Since honeybee colony maintenance is an inexpensive exercise, it is one of the major alternate income sources for the rural households. Up to May 2015, according to the statistics, 5367 entities (including the individual farmers) have registered 869220 bee colonies with the NBB; the lion share are from the states of Uttar Pradesh (26.14%), Punjab (25%), Haryana (12%), Bihar (11%), and West Bengal (7%) (Anonymous 2015). Because, they are the major producers of several oil crops, such as mustard, which attracts the honeybees. According to the United States Department of Agriculture (USDA), India is the major global exporter of the honey to the United States although the unit price paid to the Indian honey was lower than that paid to Brazil, Mexico, and Argentina. Interestingly, this variation in the prize was due to the variation in the flowers used for the honey production. The US paid $2.10 – Vol. No. 23(3) : March, 2017 7

$2.48/pound for the honey produced out of Orange blossoms from the above-mentioned countries. India exports honey produced from the mixed flowers and Mustard flowers, which was valued $0.88 (Mustard) – $ 0.94 (mixed flowers) per pound (Anonymous 2017). According to USDA (Anonymous 2017) India receives about 70 million US dollars as the revenue from the honey export to the United States alone. This shows the tremendous potential in expanding apiculture and producing good quality honey by using the colonies in other major plantation or monoculture crops. However, it might be required to reduce the pesticide use at least during the blossom period of the crop plants, as honeybees are negatively affected by the pesticide use. Although the Ministry of Agriculture and the associated institutions in India have been promoting the bee culture from the perspective of honey production and the revenue expected from the honey export, India has given very little attention to value the honeybees and other wild bees as the pollinators of our crops. Pollination is the transfer of viable pollen from the dehisced anthers to the receptive stigmas, and is a fundamental requirement for the sexual reproduction in flowering plants. The number of ovules and the proportionate number of compatible and viable pollen grains arriving to the stigma of a flower determine the pollination level in flowers. It has been assessed in terms of the fruit set, seed set, seed quality (viability of the seeds) and fruit quality (size, form, nutritional value etc.). It is therefore directly related to yield for all crop plants that are benefited from sexual reproduction. About 20,000 species of wild bees and some species of butterflies, moths, wasps, beetles, birds, bats and other vertebrates contribute to pollination in plants. The global data on crop pollination showed that 75% of the crop plants depend fully or greatly benefited from the visits of the animal pollinators in pollination process. Therefore, the service is estimated to have a global annual value between $ 235 billion and $ 577 billion. For instance, the IPBES valued the service of pollinators for Apple production to $ 33.5 billion/year, for mangoes up to $ 14.8 billion/year, and for almonds up to $ 3.5 billion/year. There is a global concern that the pollinators are declining, although that assessment is still skeptical and controversial subject among the stakeholders. Researchers who support this viewpoint have performed their studies in the developed parts of the world, particularly in the northern and western hemispheres of the globe that support relatively less biodiversity and depend the managed honeybee colonies for the pollination services. Also, the crops they grow are honeybee dependent. Those who oppose this viewpoint do so for the same fact that these reports are coming from the crops that depend managed honeybees for pollination service, and it should not be perceived as a global trend. However, there is a consensus among the world authorities that the managed honeybee colonies are declining and their visit rates to the crop flowers are dwindling. The steady decline of honey production from the managed honeybees vouches this argument. The reasons for the European honeybee (Apis mellifera) colony reduction are: a) habitat loss and fragmentation, b) land-use change, c) variation in flower production, d) diseases and pests, e) pesticide use in the crop plants and toxicity, f) global honey trade, and g) climate change. While most of these factors have direct impact to the honeybee colonies, some factors have interactive effects and indirect effects on honeybee decline (Smith et al. 2013; Muli et al. 2014; Otto et al. 2016; Fairbrother et al. 2014). The trend is not different for the other managed bees, such as stingless bees (Koffler et al. 2016). Interestingly, some studies from the tropical parts of the world have shown that beehive numbers, therefore the honey production have increased at an average rate of 3.9% and 12.97%, respectively during the period 1997-2011 (Yimer 2014). Ethiopia alone had reported 165 times growth in the quantity of the honey produced and 97 times growth in the revenue generated from the honey export between the period 1997 – 2011 (CSA 2006). This indirectly suggests that the crops benefited from the honeybee visits are unlikely to be affected in the southern hemisphere of the world, particularly in the tropics. The third argument is that it is not the bee populations that have declined, but the pollinator-dependent crops have increased by 300 per cent over the last five decades, but the pollinator population has not increased in the same way (Aizen et al. 2008). Peoples' food habits have changed a lot; for instance in the case of coffee, a crop that benefits greatly from honeybee visits, the consumption has increased steadily (Fulgoni III et al. 2015), but, the yield has not. The pollinator-dependent crops are costlier than the non-pollinator dependent crops (IPBES 2016); because, world's most important cash crops are pollinator-dependent (for instance, coffee, cocoa, almond, and cardamom). The IPBES report suggests that India should have depended pollination service for a better market value of their crops. India, since the original land of many globally-demanded spice crops and that almost all of them require animal vectors for performing pollination, it is not surprising that India has a pollinator-dependent agricultural economy. Like other Fig. 1. A worker bumblebee of Bombus haemorrhoidalis carries pollen tropical parts in the southern hemisphere, India also lacks a long-term grains of Amomum subulatum on the thorax of the bee. monitoring of our both managed and wild pollinators in crops or other plants, which limit us to suggest the temporal trend of our pollinators (LeBuhn et al. 2016). The situation in India is still grave as we know very little about the pollinators of our major crop plants. For instance, when we initiated the study of pollinators of large cardamom (Amomum subulatum) the only knowledge that we had was that honeybees are the pollinators of the crop species; but, this information was 8 ENVIS Newsletter generated based on the observation that the honeybees were harvesting pollen from the flowers. Our rigorous observations in the flowers for three years in Sikkim and Darjeeling parts of the Himalayas showed that the honeybee is a pollen robber rather than the pollinator of the large cardamom (Sinu and Shivanna 2007; Sinu et al. 2011; Sinu 2011). We found that bumblebee is the major pollinator of the crop in the Himalayas (Fig. 1). The global estimate shows that nearly 90% of wild species depend fully or in part, the animals, for pollination. We know almost nothing about the pollinators of our wild plants, the information on pollinators of the wild plants are either too less for a megabiodiverse country like India or only very superficial information is available. It is very unfortunate that India despite a home for the two mega biodiversity hotspots and several endemic species and shares the plants of two ecologically and evolutionarily important continents, have no specific programs to monitor pollinators for wild and crop plants. Since insects are the major pollinators of tropical plants, collaborative researches between plant reproductive biologists, insect ecologists and taxonomists might be required to advance our knowledge on pollination ecology of our crop and wild plants. ACKNOWLEDGEMENTS The author is grateful to Kerala State Economic and Planning Affairs, Trivandrum for funding the research in production landscapes. REFERENCES Aizen MA, Garibaldi LA, Cunningham SA, Klein AM (2008). Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Current Biology 18: 1572–1575. Anonymous (2015). State wise details of beekeepers registered with the National Bee Board up to May 2015. http://nbb.gov.in/pdf/registered_beekeepers_May2015.pdf (accessed on 11 March 2017) Anonymous (2017). National honey report. United States Department of Agriculture. Number 37-2. www.ams.usda.gov/mnreports/fvmhoney.pdf (accessed on 11 March 2017) Bailes EJ, Ollerton J, Pattrick JG, Glover BJ (2015). How can an understanding of plant-pollinators interactions contribute to global foods security? Current Opinion in Plant Biology 26: 72–79. CSA (Central Statisitcal Authority) (2012). Agricultural sample survey. Addis Ababa, Ethiopia (accessed through Yimer 2014) Chaplin-Kramer R et al. (2014). Global malnutrition overlaps with pollinator-dependent micronutrient production. Proceedings of Royal Society B, 281. e20141799. Fairbrother A, Purdy J, Anderson T, Fell R (2014). Risks of neonicotinoid insecticides to honeybees. Environmental Toxicology and Chemistry 33: 719–731. Fulgoni III VL, Keast DR, Leiberman HR (2015). Trends in intake and sources of caffeine in the diets of US adults: 2001–2010. Garibaldi LA et al. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society of London B: Biological Sciences 274: 303–313. Koffler S et al. (2015). Temporal variation in honey production by the stingless bee Melipona aubnitida (Hymenoptera: Apidae): long- term management reveals its potential as a commercial species in Northeaster Brazil. Journal of Economic Entomology 108: 858–867. LeBuhn G et al. (2016). Monitoring pollinators around the world. In Pollination Services to Agriculture: Sustaining and Enhancing a Key Ecosystem Service. pp 3–16. Moritz RF, Erler S (2016). Lost colonies found in data mine: global honey trade but not pests or pesticides as a major cause of regional honeybee colony declines. Agriculture, Ecosystems & Environment 216: 44–50. Muli E et al. (2014). Evaluation of the distribution and impacts of parasites, pathogens, and pesticides on honey bee (Apis mellifera) populations in East Africa. PloS One 9: e94459. Otto CR, Roth CL, Carlson BL, Smart MD (2016). Land-use change reduces habitat suitability for supporting managed honey bee colonies in the Northern Great Plains. PNAS USA 113: 10430–10435. Sinu PA, Shivanna KR (2007). Pollination biology of large cardamom (Amomum subulatum). Current Science 93: 548–552. Sinu PA (2011) Bumblebee pollination in large cardamom of Sikkim Himalaya. Current Science 107: 828–829. Sinu PA, Kuriakose G, Shivanna KR (2011) Is the bumblebee (Bombus haemorrhoidalis) the only pollinator of large cardamom in central Himalayas, India? Apidologie 42: 690–695. Smith KM, Loh EH, Rostal MK, Zambrana-Torrelio CM, Mendiola L, Daszak P (2013). Pathogens, pests, and economies: drivers of honey bee colony declines and losses. EcoHealth 10: 434–445. Yimer KM (2014). Assessment of beekeeping practices and honey production in Mejhengir zone of Godere district, Gambella people national regional state, Ethiopia. M.Sc. thesis submitted to Haramaya University. Vol. No. 23(3) : March, 2017 9

ECOSYSTEMS SERVICES PROVIDED BY DUNG BEETLES Sabu K. Thomas1* and Nithya Sathiyandran2 Post Graduate & Research Department of Zoology, St. Joseph's College, Devagiri, Calicut, Kerala, India 673008 E-mail: [email protected] , [email protected] *Corresponding author

INTRODUCTION Dung beetles of the subfamily are a functionally important group of soil dwelling insects that survive mainly on the dung from mammals. Additionally they feed on decomposing matter, carrion, decaying fruits and fungi (Hanski and Cambefort 1991). They locate dung from a distance with the aid of odour emanating from the dung for their breeding and feeding activities and it leads to removal of dung from soil surface. Most dung species compete for the scarce and short-lived dung droppings of mammals. As fresh dung pats are not easily available, there is intense competition among the dung beetles for fresh dung. Different functional and temporal guilds, variations in biology, differences in food searching behavior and dietary specificity of the dung beetles are the mechanisms employed by dung beetles to increase resource sharing among dung beetle species and also to protect the food from adverse environmental conditions. It has lead to three major forms of dung removal strategies by the dung beetles and formation of three functional guilds of dung beetles such as, rollers, tunnellers and dwellers. Dung beetles, known as rollers (telecoprid nesters), roll dung balls away from the dung pat, and then will pack it into the end of a tunnel, which are used as a food source or brooding chambers. Dung beetles of the dweller guild (endocoprid nesters) simply live in manure. Dung beetles, known as tunnellers (paracoprid nesters), and build tunnel beneath the dung pat, which they fill with a small dung ball to use as a food for their developing offspring. Members of tunnellers and rollers lay eggs in the dung balls and dwellers in the dung pat itself. The larvae develop and pupate within the brood balls, and emerge as adults (Halffter & Edmonds 1982). Additionally, most species of rollers and tunnellers make feeding balls those are buried and may be abandoned uneaten. Dung accumulation and dung removal by dung beetles are integral part of their feeding and breeding behaviour. Activities associated directly and indirectly with dung removal and burial by dung beetles can be considered to be ecosystem services, because of their potentially large economic importance and positive impacts on human welfare (Nichols et al. 2008) which remains poorly recognized in India. The various ecosystem services provided by dung beetles are dung removal and dung decomposition; suppression of dung breeding pests and parasites; improving nutrient recycling and improvement of soil structure; secondary ; regulation of seed predation; and limiting the emission of greenhouse gases associated with animal waste and cattle farming (Bang et al. 2005; Yamada et al. 2007; Gronvold et al. 1992; McKinney and Morley 1975; Bergstorm et al. 1976; Andresen 2002; Pentilla et al. 2013).

ECOSYSTEM SERVICES 1. Dung removal and dung decomposition: Dung beetles arrive at dung pats attracted to the odour of the fresh dung and shred the dung pats into fragments and move dung underground by their dung removal related activities and facilitate decomposition and make the nutrients available to other organisms. Dung beetles follow grazing animals closely and within hours of defecation, the dung is disintegrated, removed from the surface and carried deep into the soil below. Dung beetles are one of the most important invertebrate contributors to dung decomposition in both temperate and tropical agricultural grasslands (Gittings et al. 1994; Lee & Wall, 2006; Kaartinen et al. 2013; Horgan, 2001; Davis 1996; Slade et al. 2011). In tropical regions, dung beetles can remove the majority of a fresh dung pat within the first few days after deposition whereas in temperate conditions, a substantial fraction will remain throughout the grazing season. Non-removal of dung pats and pellets has the potential to fowl water bodies leading to toxic algal blooms and microbial contamination, to create rank pasture in grazing fields and fertile breeding zones for pests and parasites (Forgie et al. 2013; Edwards and Pavri 2007; Brown et al. 2010, MacLusky 1960). Most dung beetles in the south west India is nocturnal and some are diurnal and some species present are during both day and night time (Sabu 2011). A number of countries that farm livestock on a large scale (Australia, USA, New Zealand and Brazil) have benefited from importing pastoral dung burying beetles for removal of dung from the pastures (Ferrer- Paris and José 2014; Hughes 1975; Grant Guilford 2013; Bornemissza 1976). It is reported that the assistance of dung beetles annually saves the United States of America approximately $380 million within their cattle industry, through simply burying livestock feces (Losey and Vaughan 2006). 2. Suppression of dung breeding pests and parasites: Dung removal by dung beetles protect livestock. Many pests and parasites breed within cattle dung, particularly flies and worms, which can have harmful effects on livestock. Accumulation of fresh dung could provide habitat for hook worms and nuisance flies such as biting stable flies, blow files, house flies, and flesh flies. Dung beetles protect livestock through the process of dung removal, as well as being a competitor to these pests (Blume et al. 1973; Bornemissza 1970; Nichols et al. 2008). Survivorship of fly eggs and larvae is significantly reduced by rapid conversion of the dung resource and mechanical damage during dung manipulation by the beetles. Shredding of the dung pats leads to drying up of dung fragments and death of parasite eggs and larvae faster than in dung pats without beetles. Many laboratory and field experiments confirm significant reductions in the numbers of 10 ENVIS Newsletter dung breeding pest flies because of dung beetles (Doube et al. 1988). Competition between dung beetles and pest species occurs due to a combination of factors including, brood ball production limiting resources for older fly larvae. Fly and pest eggs or larvae can also be directly damaged by the feeding of dung beetles (Ridsdill-Smith et al. 1987; Bishop et al. 2005). Deep burial of dung reduces vertical migration by parasite larvae back upto the soil surface. There have been no assessments of the dung beetle mediated suppression of pests and parasites from the Indian mainland. 3. Improving nutrient recycling and soil structure: Dung beetles, as well as other burrowing insects, rearrange the soil and sediments by the process of bioturbation (Edwards & Achenborm 1987; Scholtz et al. 2009). Bioturbation, which is the mixing and redistribution of sediments, is an important process that affects soil moisture and soil aeration. Among the 3 functional guilds of dung beetles, tunnelers are especially important for bioturbation. Tunnelling and dung burial result in increased grass root growth and biological activity in soils under and adjacent to dung pats. Tunneling activity moves large amounts of soil to the surface and therefore increases water and root penetration and soil aeration, thus reducing run-off. Nutrient rich material from dung is relocated to upper soil layers, which is important for plant growth in an agro-ecosystem. Biomass of plants grown in soil with dung worked by dung beetles increase due to the role of dung beetles in nutrient mobilization (Nichols et al. 2008; Scholtz et al. 2009, Brown et al. 2010). Increasing the dung beetle population on pastures by introduction of dung beetle species would be very beneficial for forage production in high density grazing systems. Numerous experiments and researches have indicated that the yields of plants increase significantly through the presence and action of dung beetles (Fincher et al. 1981, Scholtz et al. 2009). Hence introduction of dung beetles and promoting agricultural and animal husbandry activities that lead to dung population build up should be part of the organic farming practices which is becoming popular in Indian agricultural scenario. It necessitates identification of the local prominent dung beetles with high fecundity in each region as the first step. 4. Seed dispersal, seed burial and preventing seed predation: Dung beetles have an important role in seed dispersal. Seeds swallowed by frugivorous mammals are often defecated intact and are viable. Most of the seeds defecated onto the surface of the soil may be destroyed by rodents or other seed predators unless buried. This burial is accomplished almost entirely by dung beetles. Dung beetles along with their dung burial activity aids in the seed burial, seed dispersion and limiting the seed predation of many plants (Estrada & Coates-Estrada 1991, Andresen 2002, Andresen and Levey 2004). Rollers and tunnellers make feeding balls with dung from the grazing and browsing mammals (cow, buffalo, sheep in agriculture landscape; boar, elephants, gaur, monkeys and deer in forest landscape) most of which often contains seeds of various plants mostly of herbs and shrubs. Seeds present in dung balls are abandoned by the beetles deep in their burrows. It leads to the burial of seeds present in the dung of mammals which otherwise might have remained on soil surface and might have been picked by seed eaters like rodents and birds and granivorous insects. Seed dispersal can occur vertically, via tunneling beetles, or horizontally, by rolling species (Nichols et al. 2008). Endozoochory by beetles facilitate the dispersal of viable seeds after passage through the gut away from the parent plant to potentially favourable underground sites offering a high probability of germination and establishment success (Vega et al. 2011). The two-phase dispersal event in which dung beetles move seeds after endozoochory is often assumed to be advantageous for plant regeneration as seeds are expected to end up in favourable and safe germination sites. There are no other insects or arthropods undertaking burial of seeds associated with dung in soil ecosystem. Dung beetles have an importance role in reforestation as secondary seed dispersers and seed burial agents as they can get seeds to the lower layers of soil which primary seed dispersers such as birds, bats and monkeys are unable to do. Evolution of the most extreme case of seed dispersal is shown by the plant Ceratocaryum argenteum where the plant exploits the visual and olfactory sensory perception of a dung beetle for dispersal and burial of its seeds (Midgley et al. 2015). The seeds are similar in appearance to dung pellets. Seeds emit many volatiles found to be present in herbivore dung which attracts beetles mistaking it as dung and the beetles that roll and bury them. As the seeds are hard and offer no reward to the dung beetles, this is a remarkable example of deception in plant seed dispersal. 5. Limiting the emission of greenhouse gases: It is likely that the dung removal and burial into lower soil layers will reduce the production of methane and nitrous oxide, and therefore decrease the emission of greenhouse gases associated with animal waste. Experimental studies (Pentilla et al. 2013) have shown that dung beetle activity during feeding and nesting will stimulate aerobic conditions, altering the microorganism fauna in dung pats, brood balls and associated soils to reduce methane production. Above studies indicate that the dung beetles living in cow pats may reduce emissions of the key greenhouse gas – methane and further exploration of the subject by conducting field studies are needed to reach at conclusions. 6. Ecology of Indian dung beetles: India with its large agriculture base and world's largest population of dung producing livestock has a huge population and diversity of dung beetles in the different biogeographic zones of the country. Agricultural and livestock activities have been benefitted from the ecosystem services provided by dung beetles for many centuries. Before the arrival of modern sanitary facilities, dung beetles were the major dung removers in rural belts. Dung beetles have been declining rapidly throughout temperate and tropical ecosystems due to changes in agricultural practices, including intensification and reduced pasture grazing, habitat loss, and overuse of anthelmintics (dewormers). Among the 137 dung beetle species reported prior to the habitat modification of the moist south Western Ghats, only 87 species were recorded in the recent collection efforts (Sabu et al. 2011). Non-record of 50 species indicates Vol. No. 23(3) : March, 2017 11 that they are either extirpated or have become rare after the habitat modifications. The research efforts though very few on the ecology of the Indian dung beetles (Mittal 2005; Mittal and Kakkar 2005, Sabu 2011; Sabu et al. 2011, Venugopal et al. 2012, 2014) indicate that though the taxonomy of the group is well known, dung beetles remain as a least recognized beneficial soil organism in India. Understanding their various roles in the agriculture and forests landscape will reveal how even seemingly insignificant organisms can have important roles in ecosystem function. Awareness is to be created about the need to protect them from extinction. Understanding the ecological role of dung beetles requires field studies in the natural and agricultural belts. Modern agricultural and livestock rearing practices, including intensification of agriculture and reduced pasture grazing and habitat loss have lead to considerable decline of dung beetle populations in the agricultural belts across India. Hence studies in natural forest landscape are essential to understand the native dung beetles. It involves considerable operational effort for locating fresh dung in the forest landscape in the early morning and late evening hours for the dung baited pitfall traps and the retrieval of the pitfall traps not disturbed by wild animals after a few days and taxonomic verification of the collected specimens with the limited expertise available. However, denial of forest collection permissions and issuing permission for photography alone for government approved research projects by various state forest departments is a subject of great concern that makes dung beetle ecology studies impossible.

ACKNOWLEDGEMENTS Financial assistance provided by UGC (University Grants Commission, India) to study the community ecology and biosystematics of dung beetles in the South Western Ghats during 2012-2015 is gratefully acknowledged.

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Major dung beetles in the south western Ghats Tunnellers 1) Caccobius (Caccophilus) meridionalis Boucomont 1914 2) Caccobius (Caccophilus) ultor Sharp 1875 3) Caccobius (Caccophilus) vulcanus (Fabricius 1801) 4) Catharsius (s.str.) molossus (Linnaéus 1758) 5) Cleptocaccobius arrowi Cambefort 1985 6) Copris (s.str.) repertus Walker 1858 7) Onthophagus falsus Gillet 1925 8) Onthophagus madoqua Arrow 1931 9) Onthophagus ( Colobonthophagus) dama (Fabricius 1798 10) Onthophagus (s.str) rectecornutus Lansberge 1883 11) Onthophagus (s.str.) andrewesi Arrow 1931 12) Onthophagus (s.str.) bronzeus Arrow 1907 13) Onthophagus (s.str.) centricornis (Fabricius 1798) 14) Onthophagus (s.str.) ensifer Boucomont 1914 15) Onthophagus (s.str.) fasciatus Boucomont 1914 16) Onthophagus (s.str.) furcillifer Bates 1891 17) Onthophagus (s.str.) pacificus Lansberge 1885 18) Onthophagus (s.str.) turbatus Walker 1858 19) Paracopris signatus (Walker 1858) Rollers 1) Sisyphus (s.str.) longipes (Olivier 1789 2) Sisyphus (s.str.) neglectus Gory 1833 Dwellers 1) Tibiodrepanus setosus (Wiedemann 1823) 2) Tiniocellus spinipes (Roth 1851)

ECOSYSTEM SERVICES OF ANTS Rasneet Lobana Ant Systematics and Molecular Biology Lab., Department of Zoology and Environmental Sciences, Punjabi University Patiala, Punjab, India,147002 Corresponding author: [email protected]

INTRODUCTION Ants are conceivably the planet's most copious eusocial insects of the family Formicidae, belonging to order Hymenoptera. Living ants are presently classified into 17 subfamilies, 334 genera, 13235 species (Bolton 2017). From Indian subcontinent, 10 subfamilies, 100 genera and 830 species have been described till date (Bharti 2017). Ants advanced from wasp-like ancestors in the mid-cretaceous period between 110 and 130 million years ago and diversified thereafter (Brady et al. 2006; Moreau et al. 2006). Ants have been known to form colonies that range in size from a few dozen predatory individuals living in small natural cavities to greatly organised colonies that may occupy outsized territories and consist of millions of individuals. Ants have colonised almost every landmass on Earth occupying a grand array of habitats. Additionally, ants thrive in most ecosystems and form 15-25% of the terrestrial animal biomass. Almost certainly, 87% of the currently classified ants belong to four major ant subfamilies, namely , Formicinae, Ponerinae and Dolichoderinae (Guenard 2013). Their accomplishment in a gigantic milieu has been ascribed to their societal organisation, phenotypic agility coupled with robustness of genotype and their knack to modify habitats, tap resources, and shield themselves. Furthermore, ant societies include division of labour, communiqué amid individuals, and an aptitude to unstitch intricate problems. Ecosystem is a multifarious network of interconnected systems. It is basically defined as a complex of interactions not only among the various organisms, but also between the organisms and their surroundings. Ants genuinely play a marvellous part in the environment as they are round about present at all the trophic levels of food web. Besides, they have a multifold effect on their local ecosystem which influence altogether the density, diversity, function and behaviour of other species just about them. They act as soil turners, tunnel builders, 14 ENVIS Newsletter scavengers, predators, seed harvesters, honeydew feeders, fungus growers, herbivores and biological pest control agents etc. Subsequently, their multifaceted role in the ecosystem has truly grabbed them the title of "Ecosystem Engineers" in broad. The ensuing section of the article step-wise brings into picture the bionetwork of ants in conjugation with other life forms. ANTS AS SOIL TURNERS Ants influence the level of nutrients in the soil by stirring the soil all through nest building movement and while gathering food. Ants move in the various chambers of their nest thereby turning and ventilating the soil, allowing water and oxygen to reach plant roots more effectively. This can indirectly impact the local populations of many animal groups, from decomposers such as Collembola, to species much higher up the victual chain. As an outcome of the foraging bustle, ants radically augment and modify the chemical properties of the soil with a constant flow of organic materials. Consequently, there is an alteration in soil moisture, pH, temperature, potassium, calcium, other ions, etc. ANTS AS PREDATORS Ants prey on a wide range of other animals, including generously proportioned prey which can be attacked by vast numbers of ant workers. Dirk Sanders, an author of the study from the university's Centre for Ecology and Conservation, said: "Ants are very effective predators which thrive in huge numbers. They're also very territorial and very aggressive, defending their resources and territory against other predators. All of this means they have a strong influence on their surrounding area". Army ants belonging to genera Aenictus and Dorylus assail the prey en masse. Army ants can devour upto 1,00,000 prey animals each day and thus have a momentous influence on the population, diversity and behaviour of their prey. Army ants on the tread are known to kill tethered horses, human babies, lizards, snakes, chickens and small mammals. Genus Oecophylla or weaver ants are canopy ants that prey on small insects and tend the . They also hold splendid architecture and astute to assemble their nests by means of leaves. ANTS AS INDICATORS OF ECOSYSTEM HEALTH A bioindicator is any biological species or group of species whose function, population, or status can divulge the qualitative status of the environment. Invertebrates make good indicators of ecological condition because they are highly diverse and functionally important, can integrate a variety of ecological processes, are sensitive to environmental change, and are easily sampled (Greenslade & Greenslade 1984; Brown 1997; McGeoch 1998). Ants have been extensively used to explore the impinge of anthropogenic activities on the functioning of the ecosystem. They have been worked out to unravel the effect of human land-use on the diversity of flora and fauna of a region. Ants comprising genera Lepisiota, Carebara, , Polyrhachis have been made use as indicators of ecosystem goodness. An extensive study via ants as indicators of ecosystem wellness was carried out and the findings point towards a distressed, sullied ecosystem with high anthropogenic impact and reduced ecosystem health, even in the primary and protected forest areas. It was also established that invasive species pretence a stern threat to the native species of Himalaya (Bharti et al. 2016). ANTS AS BIOLOGICAL PEST CONTROL AGENTS Ants perform many ecological roles that are positive to humans, including the containment of pest populations. The weaver ants Oecophylla have been comprehensively used in citrus cultivation in Southern China and it's probably considered as one of the oldest known applications of biological control. In Nicaragua, ants have been incorporated as a module of an integrated pest management program on maize as they were appreciably found to reduce fall armyworm and corn leafhopper profusion that potentially used to damage maize plants. (Perfecto 2014). A keystone ant species Azteca sericeasur has been used as a proficient biological control of coffee berry borer (Hypothenemus hampei), a notorious and economically detrimental pest of coffee identified globally. Cashew yields 49% higher in plots controlled by ants over those controlled with traditional chemicals. Australian mango crops using ants as biocontrol had a net income that was 73% higher. Dorylus, the driver ants have a propitious impetus on the lives of African farmers, ridding their fields and homes of an array of pest species from termites to rats. ANTS AS HONEYDEW FEEDERS Aphids and other hemipteran insects secrete a saccharine fluid called honeydew, when they feed on plant sap. The sugars in honeydew are a high-energy food source, which many ant species (Crematogaster peringueyi) collect as a nutrient. In some cases, the aphids secrete the honeydew in retort to ants tapping them with their antennae. The ants in turn keep predators away from the aphids and in addition move them from one feeding location to another. Ants have also been known to tend to reap their honeydew.

ANTS AS POLLINATORS AND SEED HARVESTERS Seed dispersal by ants or myrmecochory is widespread and fresh estimates suggest that nearly 9% of all plant species may have such ant associations. Several plants in fire-prone grassland systems are particularly dependent on ants for their survival and dispersal as the Vol. No. 23(3) : March, 2017 15 seeds are transported to safety below the ground. Many ant-dispersed seeds have special external structures, elaiosomes, that are sought after by ants as food. Ants of subfamily Myrmicinae belonging to genera Messor, Pogonomyrmex and Pheidole work as excellent seed harvesters and dispersers. ANTS AS FUNGUS GROWERS Ant- fungus association is an established example of symbiosis. Fungus-growing ants or leaf-cuttings ants as they are frequently entitled, belong to two chief Attine genera Atta and Acromyrmex (Guenard 2013). Fungus-growing ants that formulate the tribe Attini, promulgate certain species of fungus in the Leucoagaricus genera of the Agaricaceae family using plant leaves as a substrate. In this ant- fungus mutualism, both species depend on each other for continued existence, where an ant cultivates a fungus and the fungus serves as a food for the developing ant larvae. Interestingly, fungus cultivation is not only confined to higher attines, but lower attines of the genera Apterostigma, Cyphomyrmex and Myrmicocrypta also propagate fungus using a different substratum (insect body remains). ANTS AS FOOD Strange as it would sound that a miniature organism like ant can be used as food. Ants and their larvae are consumed in diverse parts of the world. The eggs of some of the ant species are used in Mexican cuisine. Surprisingly, in some regions, large-bottomed ants Atta laevigata are toasted alive and eaten. In not many regions of India, but throughout Burma and Thailand, a paste of the green weaver ant (Oecophylla smaragdina) is served as a condiment with curry. Weaver ant eggs and larvae, as well as the adults, are used in a Thai salad, yam in several regions of Thailand. CONCLUSION Ants are tiny yet so miraculous creatures executing countless chores which are herculean compared to their size. Ant colonies are described as superorganisms as they appear to operate as a unified entity, collectively working together to support the colony (Hölldobler and Wilson 1990 & 2008). Ants have at all times astonished us by their pervasion and profusion in a multitude of spheres from implausible predators to a gauge of ecosystem well-being. Perchance, their triumph possibly in most of the ecosystems lie in their alliance with other flora and fauna of the ecosystem with which they are directly or indirectly linked with. The world of ants is magnificent - there are still miles to go and a great deal of facts yet to be unveiled. ACKNOWLEDGEMENTS Financial assistance rendered by Ministry of Science and Technology, Government of India, New Delhi under DST-INSPIRE PROGRAMME (Reg. No. IF 140737) is gratefully acknowledged. I am profoundly gratified to my Supervisor Dr. Himender Bharti who helped me in lettering this article. REFERENCES Bequaert J (1921). "Insects as food: How they have augmented the food supply of mankind in early and recent times". Natural History Journal 21: 191–200. Bharti H (2017). Indian ants. Accessed online at http://www.antweb.org/india.jsp. on 12th March, 2017. Bharti H, Bharti M and Pfeiffer M (2016). Ants as bioindicators of ecosystem health in Shivalik Mountains of Himalayas: assessment of species diversity and invasive species. Asian Myrmecology 8: 1–15. Bingham CT (1903). Fauna of British India. Hymenoptera 3. p. 311. Bolton B (2015). An online catalogue of Ants of the World. Antcat. http://www.antcat.org/ accessed on 12th March, 2017. Brady SG, Schultz TR, Fischer BL, Ward PS (2006). Evaluating alternative hypotheses for the early evolution and diversification of ants. Proceedings of National Academy of Sciences of the United States of America 103(48):18172–18177. DeFoliart GR (1999). "Insects as food: Why the western attitude is important". Annual Review of Entomology 44: 21–50. Guenard B (2013). An Overview of the Species and Ecological Diversity of Ants. In: eLS. John Wiley & Sons, Ltd: Chichester. DOI: 10.1002/9780470015902.a0023598. Hölldobler B and Wilson EO (1990). The Ants. Cambridge: Harvard University Press. Hölldobler B and Wilson EO (2008). The Superorganism: The Beauty, elegance, and Strangeness of Insect Societies: 1–536. W.W. Norton and Company, London. Moreau CS, Bell CD,Vila R, Archibald SB, Pierce NE (2006). Phylogeny of the Ants: Diversification in the Age of Angiosperms. Science 312:101–103. Perfecto I (2014). Ants (Hymenoptera: Formicidae) as Natural Control Agents of Pests in Irrigated Maize in Nicaragua. Journal of Economic Entomology 84 (1): 65–70. Styrsky JD, Eubanks MD (2007). "Ecological consequences of interactions between ants and honeydew-producing insects". Proceedings of Biological Sciences 274 (1607): 151–164. 16 ENVIS Newsletter

Centenary Celebration at ZSI Headquarter on July, 2016 in the presence of Hon’ble Minister of Environment and Forest: Shri Prakash Javadekar

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