WSN 153(2) (2021) 93-123 EISSN 2392-2192
Dung beetles: key to healthy pasture? An overview
Sumana Saha1,a, Arghya Biswas1,b, Avirup Ghosh1,c and Dinendra Raychaudhuri2,d
1Post Graduate Department of Zoology, Barasat Government College, 10, K.N.C. Road, Barasat, Kolkata – 7000124, India
2IRDM Faculty Centre, Department of Agricultural Biotechnology,
Ramakrishna Mission Vivekananda University, Narendrapur, Kolkata – 700103, India
a,b,c,dE-mail address: sahasumana2010@gmail.com, arghyabiswas72@gmail.com,
avirupghosh1234@gmail.com, dinendrarccu@gmail.com
ABSTRACT
Dung beetles (Coleoptera: Scarabaeidae) do just what their name suggests: they use the manure, or dung of other animals in some unique ways! Diversity of the coprine members is reflected through the differences in morphology, resource relocation and foraging activity. They use one of the three broad nesting strategies for laying eggs (Dwellers, Rollers, Tunnelers and Kleptocoprids) each with implications for ecological function. These interesting insects fly around in search of manure deposits, or pats from herbivores like cows and elephants. Through manipulating faeces during the feeding process, dung beetles initiate a series of ecosystem functions ranging from secondary seed dispersal to nutrient cycling and parasite suppression. The detritus-feeding beetles play a small but remarkable role in our ecosystem. They feed on manure, use it to provide housing and food for their young, and improve nutrient cycling and soil structure. Many of the functions provide valuable ecosystem services such as biological pest control, soil fertilization. Members of the genus Onthophagus have been widely proposed as an ideal group for biodiversity inventory and monitoring; they satisfy all of the criteria of an ideal focal taxon, and they have already been used in ecological research and biodiversity survey and conservation work in many regions of the world. The existence of distinct communities of coprophagous beetles, which differ in their species composition, species-abundance relations and efficiency of dung removal, plays a major role in the breakthrough in pasture and livestock management. They as well play roles in pollination and trophic management. The dung beetles release strategy group concluded that they also result in the reduction of greenhouse gas emitted from agricultural sector like many others;
these insects too have medicinal value. Even after the presence of high endemicity, they are still somewhat at back place in an adjunct of apt knowledge on them with very few studies done on them, the need of the hour being to utilise this potential as bioresource in the interest of society and socio- economic value. Present paper is an attempt to provide an overview on the knowledge generated and what we could do so far on the dung beetle diversity in the Dairy Farm of Ramakrishna Mission Ashrama Campus, Narendrapur, South 24 Parganas & buffaloshed Naihati, North 24- Parganas, West Bengal.
Keywords: Dung beetle, Dweller, Oniticellus cinctus (Fabricius), O. spinipes Roth, New record, West Bengal, Coleoptera, Scarabaeidae
1. INTRODUCTION
Dung beetles do just what their name suggests: they use the manure, or dung, of other animals in some unique ways! These interesting insects fly around in search of manure deposits, or pats, from herbivores like cows and elephants. Dung beetles come in a variety of colours, from dull and glossy black to metallic green and red. Ancient Egyptians thought very high of the dung beetles, also known as the scarabs (derived from their family name, Scarabaeidae).
The very basic understanding of the links between ecological functions and biodiversity is needed to assess and predict the true environmental consequences of human activities. Through manipulating faeces during the feeding process, dung beetles initiate a series of ecosystem functions ranging from secondary seed dispersal to nutrient cycling and parasite suppression (Andresen, 2002). They feed on manure, use it to provide housing and food for their young, and improve nutrient cycling, soil structure, and forage growth in the meantime. Dung beetles are important enough in manure and nutrient recycling. Many of these ecological functions provide valuable ecosystem services such as biological pest control and soil fertilization. Members of the genus Onthophagus (Scarabaeidae) have been widely proposed as an ideal group for biodiversity inventory and monitoring, they satisfy all of the criteria of an ideal focal taxon, and they have already been used in ecological research and biodiversity survey and conservation work in many regions of the world. The existence of distinct communities of coprophagous beetles, which differ in their species composition, species-abundance relations, and efficiency of dung removal, plays a major role in the breakthrough in pasture and livestock management.
They as well play roles in pollination and trophic management. The dung beetles release strategy group concluded that they also result in the reduction of greenhouse gas emitted from agricultural sector like many others; these insects too have medicinal value. Even after the presence of high endemicity, they are still somewhat at back place in an adjunct of apt knowledge on them with very few studies done on them, the need of the hour being to utilise this potential as bio resource in the interest of society and socio-economic value.
2. GLOBAL DISTRIBUTION (FIG. 1)
Dung beetles are found in all continents except Antarctica and live in farmland, forest, grassland, prairie and desert habitats. Their diversity in tropical forests and savannas is extremely high (Hanski & Cambefort, 1991a,b).
Fig. 1. Dung beetle distribution globally.
Food
The beetles mostly feed on the micro-organism rich liquid component of mammalian dung and use more fibrous material to brood their larvae (Halffter & Matthews, 1966; Halffter
& Edmonds, 1982).
Types
Based on their nesting strategies dung beetles are broadly classified into three functional groups viz. rollers (telocoprid), tunnelers (paracoprid) and dwellers (endocoprid) (Figs. 2 & 3).
Three behavioral groups of the beetles are relevant to manure recycling. Probably the best- known group are the (a) tumble bugs or rollers (e.g., the species Canthon pilularius). The typical behavioural characteristic of this group is, a male female pair rolls a ball of dung (brood ball) away from a manure pile in order to bury it. Dung beetles generally work in pairs. Another group are the (b) tunnelers.
An example of this group is Onthophagus gazella, which typically bury the dung balls under the manure pat or close to the edge. Piles of soil next to the dung pat are indicators of tunneler-type dung beetle activity. Collectively, tunnelers and tumblers are classified as nesters because of their behavior in preparing a home for their young. The third group of beetles that use dung are the (c) dwellers.
Most dwellers belong to the subfamily Aphodiidae (Fig. 4). They live within the manure pat, engage in little to no digging, and generally do not form brood balls.
Fig. 2. Dung beetle types.
Fig. 3. Diagrammatic view of nests of dung beetles
Fig. 4. Species-specific groups.
3. MORPHOLOGY
The subfamily Scarabaeinae is the large insect group exhibiting extreme diversity in size (2 mm – 60 mm). Most of them are black, but a few more flamboyant species coming brown to red and brilliant shades of green or gold. They are usually round with short winged covers (Elytra) that expose the end of the abdomen. Just below the forehead their exoskeleton forms a rounded shield-like clypeus, which covers the mouthparts. Some male members possess one or two impressive horns, which they use as weapons to fend of other male competitors.
The front legs usually have serrated edges, used for power digging. Scarabs are distinguished from other beetles by appearance of their antenna which are segmented and end with plate like oval club of 3-7 expansible leaves.
These lamellate antennae create a large surface area for detecting odors. The dung chafers form manure into a ball using its scooper like head and paddle shaped antennae (Fig. 5).
Fig. 5. How do dung beetles look?
Scarabaeine dung beetles have been repeatedly proposed as a useful group for biodiversity inventory and monitoring.
They possess all of the characteristics of an ideal focal taxon, and have already been used in ecological research and biodiversity survey work throughout the world (Halffter and Favila, 1993; Favila and Halffter 1997; Rodriguez et al., 1998; Spector and Forsyth, 1998; Davis et al., 1999; Feer, 1999; Escobar, 2000; Davis, 2001; Jankielsohn et al., 2001; Lobo et al., 2001; Davis et al., 2002; Roslin and Koivunen, 2001). Dung beetles can be more rapidly and quantitatively sampled with standardized protocols than the vast majority of other insect groups. Primarily using simple, inexpensive baited pitfall traps (Halffter and Favila, 1993; Lobo et al., 1988), even non-specialist researchers can easily and quickly provide quantitative assessments of the composition, structure, and abundances of dung beetle assemblages. Globally and locally, the species diversity of the Scarabaeinae is not overwhelmingly large. A global catalog of the subfamily, the ScarabNet Global Taxon Database, is now available online at www.scarabnet.org, which lists just over 5,700 valid species of dung beetles grouped into 225 genera (ScarabNet, 2006). At local scales, dung beetle species richness ranges from just a handful of species in the higher temperate latitudes to 75 species or more in the richest tropical forests or savannas (Hanski, 1982; Price, 2004).
It is worth comparing this total to birds’ global diversity of roughly 9,700 species and the richest tropical sites hosting several hundred species. Scarabaeines have a cosmopolitan distribution, with multi-species communities occurring on every continent (other than Antarctica), ensuring their broad geographical utility. Dung beetle communities display graded responses to a variety of ecological factors or anthropogenic disturbances including pollution, habitat modification, and habitat fragmentation (Howden and Nealis, 1975; Klein 1989; Hanski and Niemela, 1990; Lobo et al. 1998; Barbero et al. 1999; Davis et al. 1999; Galante and Cartagena, 1999; Halffter et al. 1995; Krüger and Scholtz, 1997; Davis and Sutton, 1998; Davis, 2000; Jankielsohn et al. 2001; Quintero and Roslin, 2005).
Rapid changes in dung beetle communities at sharp natural habitat ecotones have been demonstrated in a number of settings (Hill, 1996; Spector and Ayzama, 2003). Shifts in the diurnal activity, nesting behaviors, and average body size of species in communities have also been documented due to habitat disturbance (Horgan, 2005).
Behaviour
Behavioural knowledge on these dung beetle presents plastic trait complexes such as polyphenism, accounting for the bewilding diversity of forms and behaviour play a vastly unexplored role in the evolution of morphological and behavioural novelties. Males of many species of dung chafers of the genera Onthophagus and Catharsius express exuberant secondary trait such as horns. These horns develop in response to larval feeding conditions and are used as weapons in aggressive interactions and also to gain access and to mate with the female. In many species, horn expression is discontinuous, and male populations are composed of two alternative, discrete shapes.
Precisely many species exhibit polyphenism for male morphology. Both horned and hornless males of Onthophagus taurus are indeed able to recognise the presence or absence of other male siblings and respond by adjusting their investment into co-operative versus mate securing behaviour (Moczek & Nijhout, 2003) (Fig. 6A). Such condition-dependent paternal assistance may represent a mechanism by which males minimize fitness in a social environment composed of variable degrees of male-male competition for females. Facultative parental
investment is likely to evolve when a patch and ephemeral resource environment favours co- operation, while at the same time intraspecific mating competition selects for behaviours that secure mates and breeding opportunities (Trumbo and Fernandez, 1995).
Many use their poop balls to cool off around noon when the sun is at its peak, they will routinely climb atop their dung balls to give their feet a break from the hot ground (Fig. 6B).
Thermal imaging also showed that dung balls were measurably cooler than the surrounding environment probably because of their moisture content. None of the members of scarabaeid genera relocates food for nesting or prepares a brood ball or mass with provisions for the larva.
The absence of these two behaviours, present in practically all Scarabaeinae, makes one think that the behaviour of these genera is very primitive. Other species also take advantage of a large mass of dung gathered by a larger beetle. This behaviour does not require nesting given that the kleptoparasite takes advantage of the mass of dung gathered by the larger beetle. This is common in Aphodiini and has also been observed for other small Scarabaeinae. There is no nidification process (i.e., accumulation or preparation of food by the mother for the larva).
There is no food relocation prior to ovipositing.
The females use food that is available, whether it is a pat of cow dung, the compact mass of excrement buried by a sloth, the sausage or brood mass made by larger beetles, or even debris in the nests of Acromyrmex. Neither brood masses nor brood balls are prepared (as occurs in endocoprid species). The eggs are not deeply laid in the food mass, and there is no preparation of an oviposition chamber. The larva moves freely through the mass of food, digging only a few centimetres into it. During this movement, the larva does not prepare a gallery. This is, in short, the simplest resource utilization process known for a species of the Scarabaeinae, and is very similar to that observed for the majority of Aphodiini and other Scarabaeoidea that do not nest. Although it is tempting to interpret the absence of nesting as a plesiomorphic character that precedes the separation of the two main evolutionary lines of nesting in Scarabaeinae (Halffter and Edmonds, 1982), this is not corroborated by the phylogenetic analyses available at present (Vaz-de-Mello, 2003, 2007; Ge´nier and Kohlmann, 2003). The latter indicates that the mentioned group is nested within a broader group that includes genera with different types of nesting behavior: paracoprid and telecoprid of the most important apomorphies are the presence of nesting behaviour and reduced ovary.
Being well supported as part of this clade and at the same time being the only branch (or probably one of the few) with no nesting, in addition to having a sister group that do nest, is the main evidence supporting the hypothesis of the loss of the nesting behaviour. Among the roller Scarabaeinae there are several species in which nesting is missing in one or several of its characteristic traits. These behaviours are the formation of a ball of food where the food is found, and its relocation by rolling. Pachysoma MacLeay is a brachypterous genus that inhabits the deserts of western South Africa.
The female of this species (nesting process is described by Scholtz et al., 2004) collects dry pellets and small fragments of plant detritus and digs a gallery. She puts the material at the bottom of the gallery and adds more that she searches for on the soil surface. The beetle relocates the material horizontally by grasping the fragment of food with her front legs while using the other four to walk, a relocation process similar to that of some Scarabaeinae, such as the Eucraniini and Canthon obliquus Horn, from very arid zones. This behaviour is a clear adaptation to how food is found under desert conditions. The other key behaviour that has been lost is the preparation of a nest ball. South African ball-rolling dung beetles exhibit a unique orientation behaviour to avoid competition for food: after forming a piece of dung into a ball,
they efficiently escape with it from the dung pile along a straight-line path. To keep track of their heading, these insects use celestial cues, such as the sun, as an orientation reference. Here the scientists show that wind can also be used as a guiding cue for the ball-rolling beetles. They demonstrate that this mechanosensory compass cue is only used when skylight cues are difficult to read, i.e., when the sun is close to the zenith.
This raises the question of how the beetles combine multimodal orientation input to obtain a robust heading estimate. To study this, the scientists performed behavioural experiments in a tightly controlled indoor arena. This revealed that the beetles register directional information provided by the sun and the wind and can use them in a weighted manner. Moreover, the directional information can be transferred between these 2 sensory modalities, suggesting that they are combined in the spatial memory network in the beetle’s brain.
This flexible use of compass cue preferences relative to the prevailing visual and mechanosensory scenery provides a simple, yet effective, mechanism for enabling precise compass orientation at any time of the day. And with a keen spatial network, beetles are able to get dung away from piles as quickly as possible – a resource so important, scientists compare it to finding a bag of money on the street (Dacke et al. 2019).
Fig. 6. (A): Males of many species of dung chafers with exuberant secondary trait such as horns, (B): Navigation of dung beetle using milky way as a guide to steer dung.
Life cycle and nesting behaviour of dung beetle
The life cycle of dung beetles is very interesting and unique with respect to most other beetles. Most dung beetle species spend 95% of their life in dung or in the soil beneath dung pats. The only time dung beetles may be observed outside this environment is when they are searching for a new dung pat to start preparing and laying their eggs. Since each dung beetle species exhibits different adaptations to their preferred microenvironment, they have somewhat specific life cycle characteristics.
The life cycle and nesting behaviour of dung beetle is studied under laboratory conditions (Gaikwad & Bhawane, 2016). The beetle construct simple nest composed of single unbranched gallery (Fig. 7). At the bottom end of each there may be one or two brood balls lodged. The depth of brood balls constructed ranges from 6 to 22 mm. The length of brood ball ranges from 22 to 34 mm with average of 27.7 mm.
The diameter of brood ball ranges between 13-18 mm. It is observed that single pair of this dung beetle has constructed 10 to 35 brood balls in laboratory condition. The female dung beetle deposits single egg in egg chamber of brood ball. The average size of the eggs is 2.36 mm in length and 1.39 mm in diameter. Embryological developmental period is averaged of 2.38 day. The larval developmental period of the three instar stage is averaged of 31.34 days.
While the average pupae stage is of 13.46 days at laboratory temperature condition ranging from 22°C to 25°C. The adult longevity ranges between 42 to 85 days.
Fig. 7. Life cycle of dung beetle.
Beetle communities and dipteran flies colonising the beetle community
The faeces of large herbivores constitute a highly specific microhabitat, which is characterized by discontinuity and a very high rate of micro-succession. Significant physical and chemical changes occur within short periods of time (Dickinson & Craig, 1990). These changes result from the activity of the various organisms that colonize animal dung, including bacteria, protozoa, fungi, nematodes, arachnids, insects and earthworms, as well as local weather conditions. The species composition of the invertebrates colonizing animal dung are determined by several factors : physicochemical properties of the dung (moisture content and size of particles), weather conditions, soil type, exposure to direct sun light, season, the size of dung piles, interactions between species, the “age” and type of dung (Landin, 1961; Desiere, 1973; Olechowicz, 1974; Breymeyer & Zachareva-Stoilova, 1975; Holter, 2004). The faeces of ruminants in the palearctic region have been studied extensively as part of ecological studies on beetles (Koskela, 1972; Koskela & Hanski, 1977; Hanski & Koskela, 1979; Hanski &
Krikken, 1991;Wassmer, 1994; Šlachta et al. 2008), true flies (Hammer, 1941; Olechowicz, 1976), cattle dung (Wassmer, 1994; Šlachta et al. 2008), sheep dung (Olechowicz, 1974, 1976;
Sowig & Wassmer, 1994; Sowig, 1995), horse dung (Psarev, 2002) and others.
These studies encompass the effect of abiotic factors on the community structure of organisms inhabiting dung at various stages in this micro-succession, their microhabitat preferences and phenology. In cattle dung the eudominant species was: Cercyonpygmaeus (Hydrophilidae, 10.4%), the dominants: Athetasordidula (Staphylinidae, 9.1%), Anotylus tetracarinatus (Staphylinidae, 8.5%), Platystethus arenarius (Staphylinidae, 8.1%) and Acrotrichis grandicollis (Ptiliidae, 6.6%).
Dung beetles: The phoront
Many mites use other animals to arrive at suitable habitats with enough food resources that ensure high success of carried mites. The phenomenon in which one animal actively seeks out and clings to the body surface of another animal in a limited time is called phoresy. During this phenomenon, the carried animal (termed the phoretic or phoront) stops both feeding and reproduction. Phoresy results in dispersal from unsuitable habitats to the suitable better conditions for the development of the phoretic mites or their offsprings. In phoretic mite species, deutonymphs or adult females are often the phoretic stages. Many groups of predatory mites have also evolved a specialised habitat association with mammalian dung (Fig. 8).
Because of the temporally and spatially isolated nature of dung pads, these mites often disperse by phoresy on coprophilous insects that have similar habitat requirements (Krantz, 1983).
Phoresy of this type requires behavioural and life history adaptations to ensure that the dispersal stage of the mite is available and active at the time when the carrier insect is ready to leave a local habitat patch.
These adaptations have become especially complex in the case of mites associated with dung beetles of the subfamily Coprinae, which demonstrate a high level of parental brood care.
In these beetles, the female sometimes together with the male, remains in the underground nest chamber caring for the brood until the emergence of the progeny. Many species of mites that breed in these nest chambers disperse by phoresy on the beetles, as is common for other taxa of dung beetles, but the existence of brood care in the Coprinae means that the mites have the unusual opportunity of access to both the parental and progeny generations of beetles (Masan
& Halliday, 2009; Bahrami et al. 2011)
Fig. 8. Mites associated with dung beetle.
Seasonal occurrence (phenology) of coprophilus beetle
Dung is one of the fundamental returns of animal matter and energy into the nutrient and energy cycles of the planet and supports a biodiverse community, especially arthropods that contribute to decomposition (Bornemissza, 1960; Waterhouse, 1974; Fincher et al. 1981; Slade et al. 2007; Nichols et al. 2008; O’Hea et al. 2010; Wu et al. 2010; Beynon et al. 2012;
Kudavidanage and. Lekamge, 2012). Coprophilous beetles are mainly comprised of larvae and adult beetles from the families Scarabaeidae (subfamilies Scarabaeinae and Aphodiinae) and Geotrupidae (Pakaluk et al. 1995; Ratcliffe and Jameson, 2005) and adult Hydrophilidae (subfamily Sphaeridiinae) (Smetana, 1978) whose larvae are predacious. Coprophilous adult and larval beetles compete with dung inhabiting dipteran larvae for food, whereas the larvae of hydrophilid beetles are important predators on dipteran larvae. Both competition and predation by coprophilous beetles reduce the fitness of many pest species that develop within dung (Valiela, 1974; Fay and Doube, 1983; Kirk, 1992). Another benefit of dung beetles is the enhancement of soil fertility (Brown et al. 2010; Ishikawa, 2011). Dung beetles increase the rate of dung decomposition by tunnelling through dung pads and mixing dung with soil when provisioning for their offspring (Fincher et al., 1981; Miranda et al., 1998; Nichols et al., 2008;
Brown et al. 2010; Liu et al. 2012). Previous research focused on dung beetle communities in southern North America: Florida (Woodruff, 1973), Georgia (Fincher, 1975; Fincher and Woodruff, 1979), Texas (Nealis, 1977; Fincher et al. 1986; Howden and Scholtz, 1986;
Howden and Howden, 2001), South Carolina (Harpootlian 2001), North Carolina (Bertone et al. 2005). Louisiana (Radtke et al. 2008) and Arkansas (Fiene et al., 2011). Dung beetle studies from northern North America provide distributional and phenological information include studies in North Dakota (Helgesen and Post, 1967), New York (Valiela 1969; Pimsler 2007), South Dakota (Kessler et al. 1974), Minnesota (Cervenka and Moon, 1991), southern Québec (Matheson 1987; Levesque and Levesque 1995), southern Alberta (Floate and Gill, 1998;
Kadiri et al. 2014), New Jersey and Maryland (Price, 2004; Price et al. 2012) and Michigan
(Rounds and Floate, 2012). Studies that provide natural history data are essential to understand beetle biodiversity (Braga et al. 2013; Korasaki et al. 2013), monitoring and advancement of adventive species (Floate and Gill, 1998; Gollan et al. 2011; Kaufman and Wood, 2012; Rounds and Floate, 2012; Floate and Kadiri et al., 2014), for providing essential ecological information on local pasture ecosystems (Schulze et al., 2005; Qie et al. 2011; Agoglitta et al. 2012; Liu et al. 2012; Numa et al. 2012; Campos and Hernandez, 2013), and as a proxy to monitor global climate change (Menendez and Gutierrez, 2004; Wu and Sun, 2012; Wassmer, 2014).
Importance of dung beetle in nutrient cycle
There are many animals and plants that perform a vital role in the nutrient cycle of pastures, particularly in humification of cattle dung. The organisms featuring prominently in this role are insects mainly flies and beetles (Skidmore, 1991). This view is different from Putman (1983) who asserted that earthworms are the primary invertebrates of cow dung decomposition. The crucial role of the dung community is demonstrated in Australia where no native cow dung loving fauna exists. It is estimated that the undegraded dung of five cattle removes from production one acre of land per year and considerable expense is being incurred in trying to establish a cow dung community (Skidmore, 1991). Australia, USA and the ranching areas of South America are seeking to correct the unavailability of native dung fauna through establishing sustainable cow dung communities mainly beetles. Pasture land covered by undegraded cow dung is effectively non-productive since research has shown that natural degradation cannot occur in the absence of insect decomposers since fossil dung pellets have been frequently found in sedimentary rocks (Skidmore, 1991). Despite the pivotal role played by beetles in the dung humification process, they are persistently exposed to lethal chemicals as non-target insects. Pyrethroids pose the greatest danger to beetles given that they are widely used to control common tropical pests such as ticks and tsetse flies (Regional Tsetse and trypanosomiasis Control Program Report, 1997). Pyrethroids are known to kill beetles through disruption of the central nervous system and are known to be more potent at the larval stage.
Nutrient quality of vertebrate dung for the dung beetles
At the basis of a trophic web, coprophagous animals like dung beetles (Scrabaeoidea) utilise resources that may have advantages as well as drawbacks. Several studies have characterised the nutrients, eg: C/N ratios and the organic matter content for specific type of dung. Analysis of water content, C/N ratios, amino acid, neutral lipid fatty acid, free fatty acid and sterol composition can give us the adequate information on their sustenance. Dung beetles strongly depend on a resource that is scarce and patchy in occurrence. Also, some dung volatiles act as nutritional cue for dung beetles. In general, animal droppings vary in nutrient amounts, even within a species or feeding guild. Whereas higher nutrient concentrations are generally beneficial, dung beetles may face trade offs that constrain a higher preference of nutrient rich dung. The C/N ratio abundance is frequently used as an index for quality descriptions of organic substrates including dung. The C/N ratio is increased over ten- fold from carnivore dung to herbivore dung. Omnivore dung has intermediate levels. Water content plays an important role as adult dung beetles mainly use the liquid phase and its nutrients/ particles to feed on, it affects the occurrence of species and the handling of brood balls. Sterols and cholesterols play key function as they serve as components of the cell membrane as regulators of developmental genes and as precursors of different hormones (Frank, 2017).
Values of dung beetle
Due to the high sensitivity of dung beetles to habitat modification and changing dung resources, many of these ecological processes have already been disrupted or may be affected in the future. Prediction of the functional consequences of dung beetle decline demands functional studies conducted with naturally assembled beetle communities, which broaden the geographic scope of existing work, assess the spatio-temporal distribution of multiple functions, and link these ecosystem processes more clearly to ecosystem services. Dung chafers with different behaviour have different effect on ecosystem services. The maintenance of ecosystem services by them depends on diverse assemblage of dung beetle species. They are important in nutrient cycling. They facilitate decomposition and make the nutrients available to other organism. Studies have found that many soil nutrients are increased when dung beetles are present. They also help increase nitrogen mineralisation, the process by which nitrogen is converted from an organic to an inorganic form making it available for use by plants and subsequently the rest of the food web. Tunnels are specially important for bioturbation i.e.
mixing and redistribution of sediments (Fig. 9).
The process affects soil moisture and soil aeration and thus increases plant productivity.
They also help increase of plant biomass, nitrogen content and grain production. These scarabs may also contribute to plant productivity by dispersal of seeds found in dung, which lead to increased plant recruitment. Beetles are important pollinators of decay-scented flowers. Such beetles can reduce the abundance of parasites and flies that breed in the dung. After laying their eggs in the ground, the larva hatch and eat gastrointestinal parasites found in the dung, and their tunnelling action aerates the soil. These processes interrupt the lifecycle of parasite. The dung beetle destroys the parasites at no charge. The dung burial activity is remarkably disrupted by land use changes from natural forest to open agricultural area. Their presence elevated about 53% of the total dung removed and reduced about 83% and 63% of fly population and richness, respectively. Dung beetles are also used as an indicator group, because they reflect structural differences between habitats caused by forest type or human habitat modification (Klein, 1989;
Nummelin and Hanski, 1989; Hill, 1996; Davis and Sutton, 1998; Davis et al. 2001). The potential of dung beetles as indicators for disturbance has been reviewed by Halffter and Favila (1993) and McGeoch et al. (2002). In addition, the body size of dung beetles may be an important factor interacting with habitat type and may be related to the presence of large mammals (Hanski and Cambefort, 1991a,b). Smaller dung beetle species are more abundant and less habitat specific (Hanski, 1982; Hanski and Cambefort, 1991a,b).
On a pasture-management level, dung pat removal is beneficial for forage availability.
Most ruminants will not graze closely to their own species manure pats. Research has shown that the forage is palatable, but avoided because of the dung pile. Consequently, cattle manure deposits can make from 5% to 10% per acre per year unavailable. By completely and quickly removing the manure, dung beetles can significantly enhance grazing efficiency. The tunnelling behaviour of dung beetles increases the soils capacity to absorb and hold water, and their dung- handling activities enhance soil nutrient cycling. An adequate population and mix of species can remove a complete dung pile from the surface within 24 hours. As the adult dung beetles use the liquid component for nourishment and the roughage for the brood balls, the dung pat quickly disappears. If left on the surface, up to 80% of manure nitrogen is lost through volatilization; by quickly incorporating manure into the soil, dung beetles make more of this nitrogen available for plant use. The larvae use only 40−50% of the brood ball before pupating, leaving behind the remainder of this nutrient-rich organic matter for soil microbes, fungi and
bacteria to use in creating humus. The effects of vegetative cover and soil type on the abundance and distribution of scarabaeine dung beetle resulted in differentiation of the diurnal and nocturnal species and also the rate of abundance in bushveld less than that of grassland. The degree of habitat specificity varied widely between species. During overcast weather, both bushveld and grassveld species became abundant in the transitional zone. It somehow stated that light intensity is one of the characteristic by which beetles recognise bushveld and grassveld. Species turnover was highest between primary forest, cropland and secondary forest.
The results of such studies concluded on the idea that regeneration areas and certain land use system can mitigate the detrimental effects of the clearance of original vegetation (Simmons &
Ridsdill-Smith, 2011).
Fig. 9 Functional consequences of dung beetles.
Factors Affecting Dung Beetle and Their Adaptation
Dung beetles have been the subject of research on the effects of environmental disturbance caused by human activity in tropical forests (Halffter and Favila, 1993). Thus, if the structure and composition of a landscape change as a consequence of human disturbance, those changes would be expected to be reflected in the structure and composition of the dung beetle assemblages. Nevertheless, landscape configuration does influence the distribution, abundance and persistence of beetle populations as a result of reduced isolation and this, in turn, facilitates movement across the landscape matrix (Montes De Oca, 2001, Estrada and Coates- Estrada, 2002). Most studies have demonstrated that dung beetles respond negatively to the fragmentation and transformation of natural habitats (Howden and Nealis, 1975; Klein, 1987;
Davis et al. 2001, Medina et al. 2002). The results from the studies referred corroborate this to
some extent, as most of the forest species are relatively less able to tolerate the microclimatic conditions typical of open areas (Klein, 1987; Halffter et al. 1992). However, the creation of new environments such as cropland and pasture favours the presence of the few forest species that can tolerate the modification of their habitat and also allows for colonization by non-forest species that arrive from other altitudinal levels. In addition to the reduction in species richness and abundance, differences in the community species composition between both types of forest and the areas used for raising cattle and agriculture. In the anthropogenic habitats, the new component of the dung beetle assemblage is a mixture of species with the capacity to use both forest and modified areas. Like the findings of Halffter and Arellano (2002), the study has important implications in terms of the conservation and management of mountain ecosystems, as they suggest that a certain degree of landscape modification can actually increase the total number of species at a regional level. Many of the species that inhabit modified areas, particularly those used for raising cattle and growing crops, can be found at elevations of under 1000 m.s.l., as is the case of Onthophagus acuminatus, O. clypeatus group and Oxysternon conspicillatum, species typical of lowland forest, and Ontherus trituberculatus, abundant between 1000 and 1300 m.s.l. (Escobar, unpublished data).
Furthermore, the differences among habitats detected at the guild level are indicative of the roller species’ sensitivity to changes in vegetation and soil use. On the other hand, the dominance of large, diurnal species in anthropogenic habitats suggests that this group has a high competitive ability to exploit available excrement. The great majority of small species are associated with forest areas, indicating a reduced capacity to colonize new environments. The environmental matrix and spatial arrangement of various elements that make up the landscape are crucial for understanding the ways in which organisms respond to changes induced by humans (Gascon et al. 1999). Many environments act not so much as absolute barriers to species movement but as selective filters, imposing new trends in the diversity, structure and composition of species assemblages.
Sustaining Beetle Population in the Ecosystem
Beetles play an important role in maintaining pastures in a productive state. There is need for constant biological monitoring of beetle populations in pastures and create conditions conducive for their self-sustenance. Indiscriminate use of broad-spectrum chemicals should be minimized as this might have negative impacts on dung beetle populations. Sensitivity of beetle families to chemicals differs hence there is need to identify predominant beetle families in a given locality. This helps determining location specific pyrethroid concentration levels that would have less detrimental to the survival of the beetles (Bath et al., 1994).
Retrospect
The section is limited to the taxonomic account of the group, primarily because of the emphasis laid in the above paragraph. Scaraboidea is one of the largest superfamilies in the order Coleoptera and is globally known by approximately 2,200 genera and about 31,000 species (Ratcliffe and Jameson, 2013). This superfamily includes three families viz. Passalidae, Lucanidae and Scarabaeidae. The last named family includes about 91% of all scarabaeoids and includes about 600 genera and 27,800 species worldwide (Ratcliffe and Jameson, 2013). Of these 7000 are known as dung beetles. Though a well documented taxonomic work on the oriental dung beetle fauna had been carried out by Arrow (1931) and Balthasar (1963a & b),
the important contributions on the oriental scarabaeids have been made by Newton & Malcolm, 1985; Biswas & Chatterjee, 1991; Veenakumari & Veeresh, 1997; Chandra, 2000, 2008, 2009;
Chandra & Ahirwar, 2005, 2007; Priyadarsanan, 2006; Chandra & Gupta, 2012, 2013; Sarkar, 2013; Jadhav & Sharma, 2012; Ali et al., 2015; Sarkar et al., 2015; Sathiandran et al., 2015;
Kalawate, 2018 and Singh et al., 2018).
4. RESULT
Authors being unaware of any study conducted in the dairy farms of West Bengal, initiated a study to unfold the faunal spectrum of dung beetles in the Dairy Farm of Ramakrishna Mission Ashrama Campus, Narendrapur, South 24 Parganas & buffaloshed Naihati, North 24- Parganas, West Bengal. During our survey we have sampled two (2) dung beetles alongwith four (4) dung loving beetles, eight (8) dung loving flies, 17 dung associated insects of different groups, one mesostigmatic mite species from cow and buffalo dung community. Out of these, two coprophagous species, Oniticellus cinctus (Fabricius) and O. spinipes Roth under subfamily Coprinae are recorded so far from cow dung from dairy farm, Narendrapur, South 24 Parganas and buffalo dung from cattle shed, Naihati, North 24 Parganas respectively.
Oniticellus spinipes is newly recorded from the state and O. cinctus first time reported from the district (Table 1; Fig. 10).
Table 1. Arthropod Species Encountered In Different Dung Communities.
Sl.
No. Name of Species
Insects Encountered During
Survey State of Dung
In Cow Dung
In Buffalo
Dung Wet/Dry
A.
1.
Dung Beetles
Oniticellus cinctus (Fabricius) √
√ W
2. Oniticellus spinipes Roth x √ D
B.
3.
Dung Loving Insects
Sphaeridium scarabaeoides (L.) √ √ W + D
4. Sphaeridium sp. 2 √ √ W + D
5. Sphaeridium sp. 3 √ √ W + D
6. Clown Beetle [Hister unicolor L.] √ √ W + D
7. Fruit Fly : Drosophilidae : Indet sp. 1 x √ D
8. Dung Loving Fly : Lonchaeidae : Indet
sp. 2 √ √ W + D
9. Dipteran Fly : Opomyzidae Indet sp. 3 √ √ W + D
10. Dipteran Fly : Opomyzidae Indet sp. 4 x √ D 11. Dipteran Scavenger Fly : Sepsidae : Indet
sp. 5 √ √ W + D
12. Lesser Dung Fly : Sphaeroceridae : Indet
sp. 6 √ √ W + D
13. Lesser Dung Fly : Sphaeroceridae : Indet
sp. 7 x √ D
14. Dipteran Fly : Tachinidae : Indet sp. 8 x √ D
C.
15. Insects Associated with Dung
Ground Beetle [Nebria sp.] √ √ W + D
16. Ground Beetle [Dromius sp.] √ √ W + D
17. Darkling Beetle [Gonocephalum
tuberculatum Hope] x √ D
18. Scarab Beetle [Aphodius prodromus
(Brahm)] √ x W
19. Staphylinid Beetle [Paederus riparius
(Linnaeus)] √ √ W + D
20. Ant [Camponotus (Tanymyrmex)
compressus (F.)] √ √ W + D
21. Ant [Crematogaster (Acrocoelia)
hodgsoni Forel] √ √ W + D
22. Ant [Diacamma scalpratum (Smith)] √ √ W + D
23. Ant [Myrmicaria brunnea Saunders] √ √ W + D
24. Ant [Pheidole (Pheidole) nietneri Emery] √ √ W + D
25. Ant [Vollenhovia oblonga (Smith)] √ x W
26. Stink Bug [Storthecoris nigriceps
Horvath] x √ D
27. Springtail (Indet sp. 1) x √ D
28. Earwig [Forficula sp. 1] √ √ W + D
29. Earwig [Forficula sp. 2] √ √ W + D
30. Spider : Salticidae (Indet sp. 1) x √ D
31. Spider : Lycosidae [Lycosa carmichaeli
Gravely] √ √ W + D
D.
32.
Mites Associated With Dung Beetles &
Dung Loving Beetles
Glyptholaspis sp. √ x W + D
Fig. 10. Dung beetles encountered during survey.
5. CONCLUSION
Through manipulating faeces during the feeding process, dung beetles instigate a series of valuable ecosystem services. Even after the presence of high endemicity, they are still somewhat at back place in an adjunct of apt knowledge on them with very few studies done on them, the need of the hour being to utilise this potential as bioresource in the interest of society and socio-economic value.
ACKNOWLEDGEMENTS
The authors express their deep sense of gratitude to The Hon’ble Vice Chancellor, Ramakrishna Mission Vivekananda Educational and Research Institute (RKMVERI), Narendrapur and The Principal, Barasat Government College for necessary logistic support. The authors also wish to thank The Secretary & The Dean, RKMVERI, Narendrapur for necessary permission to carry out the project within the campus.
References
[1] Agoglitta, R., Moreno, C. E., Zunino, M., Bonsignori, G., and Dellacasa. M. 2012.
Cumulative annual dung beetle diversity in Mediterranean seasonal environments.
Ecological Research, 27(2): 387–395
[2] Ali S.M.S., Naeem, M. Baig, F, Shahzad, A, Zia, A. 2015. New records, distributional notes and species diversity of dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) from Pothohar Plateau of Punjab, Pakistan. Journal of Entomology and Zoology Studies, 3(3): 01-06
[3] Andresen, E. 2002a. Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography, 26: 87–97
[4] Andresen, E. 2002b.Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecological Entomology 27: 257–270
[5] Arrow, G. J. 1931. The Fauna of British India including Ceylon and Burma: Coleoptera:
Lamellicornia: Part III Coprinae. Publ. Taylor and Francis, London, 428pp.
[6] Bahrami, F., Arbabi, M. Vafaei Shoushtari, R. and Kazemi, S. 2011. Mesostigmatic mites associated with Coleoptera and biodiversity calculation of these mites phoretic on dung beetles in Golestan Province (North of Iran). Middle-East Journal of Scientific Research, 9 (3): 345-366
[7] Balthasar, V. 1963a. Monographie der Scarabaeidae und Aphodiidae der
Palaearktischen und Orientalischen Region. (Coleoptera: Lamellicornia), Verlag der Tschechoslowakischen Akademie der Wissenschaften Prag, I: 1-391, 137 figs., 24 pls.
[8] Balthasar, V. (1963b). Monographie der Scarabaeidae und Aphodiidae der
Palaearktischen und Orientalischen Region. (Coleoptera: Lamellicornia), Verlag der Tschechoslowakischen Akademie der Wissenschaften Prag, I1: 1-627, 226 figs., 16 pls.
[9] Barbero, E., Palestrini, C. and Rolando, A. 1999. Dung beetle conservation: effects of habitat and resources election (Coleoptera: Scarabaeidae). Journal of Insect
Conservation, 3, 75–84
[10] Bath, D. K. M., Heinzer-Mutz, E. M. and Elster 1994. Colonization and degradation of cattle dung: Aspects of sampling, faecal composition, and artificially formed parts, Environmental Entomology, 23: 571-578
[11] .Bertone, M., Green, J., Washburn, S., Poore, M., Sorenson, C. and Watson, W. A., 2005. Seasonal Activity and Species Composition of Dung Beetles (Coleoptera:
Scarabaeidae and Geotrupidae) Inhabiting Cattle Pastures in North Carolina. Ecology and Population Biology, 98 (3), 309-321
[12] Beynon, S.A., Mann, D.J., Slade, E.M. & Lewis, O.T. 2012. Species-rich dung beetle communities buffer ecosystem services in perturbed agro-ecosystems. Journals of Applied Ecology, 49: 1365-1372
[13] Biswas. S. and Chatterjee, S.K. 1991.Fauna of Orissa. State Fauna Series 1. Zoological Survey of India, Kolkata, 3: 243-262
[14] Bornemissza, G.F. 1960. Could dung eating insects improve our pasture? The Journal of the Australian Institute of Agricultural Science, 26: 54-56
[15] Braga, R. F., Korasaki, V., Andresen, E. and Louzada, J. 2013. Dung beetle community and functions along a habitat-disturbance gradient in the Amazon: A rapid assessment of ecological functions associated to biodiversity. Plos One, 8(2): e57786
[16] .Breymayer, A. and Zachaireva-Stoilova, B. 1975. Scarabaeidae in two mountain pastures in Poland and Bulgaria. Bulletin of the Polish Academy of Science (Sci. Biol.
II), 33: 173–180
[17] Brown, J., Scholtz, C. H., Janeau, J. L., Grellier, S. and Podwojewski, P. 2010. Dung beetles (Coleoptera: Scarabaeidae) can improve soil hydrological properties. Applied Soil Ecology, 46(1): 9–16
[18] Campos, R. C., and Hernandez, M. I. M. 2013. Dung beetle assemblages (Coleoptera, Scarabaeinae) in Atlantic forest fragments in southern Brazil. Revista Brasileira De Entomologia, 57(1): 47–54
[19] Cervenka, V. J. and Moon, R. D. 1991. Arthropods associated with fresh cattle dung pats in Minnesota. Journal of the Kansas Entomological Society, 64(2): 131–145 [20] Chandra, K. 2000. Inventory of scarabaeid beetles (Coleoptera) from Madhya Pradesh,
India. Zoos’ Print Journal, 15(11): 359-362
[21] Chandra, K. 2008. Insecta: Coleoptera. In: K. Chandra (Ed.) Faunal Diversity of
Jabalpur District, Madhya Pradesh. Publ. Zoological Survey of India, Kolkata: 159-186 [22] Chandra, K 2009. Insecta: Coleoptera. In: K. Chandra (Ed.) Fauna of Pachmarhi
Biosphere Reserve. Conservation Area Series, 39: 259-299, Publ. Zoological Survey of India, Kolkata.
[23] Chandra, K. and Ahirwar, S.C. 2005. Scarabaeid Beetles of Bandhavgarh National Park, Madhya Pradesh. Zoos’ Print Journal, 20(80): 1961-1964
[24] Chandra, K. and Ahirwar, S.C. 2007. Insecta: Coleoptera: Scarabaeidae, Fauna of Madhya Pradesh (including Chattisgarh). State Fauna Series, 15(Part-1): 273-300 [25] Jerzy Borowski, Adam Byk, Tomasz Mokrzycki, Beetles (Coleoptera) of the Rogów
region. Part IX – superfamily Scarabaeoidea: Bolboceratidae, Geotrupidae, Lucanidae, Trogidae and Scarabaeidae. World Scientific News 44 (2016) 123-142
[26] Subhankar Kumar Sarkar, Sumana Saha, Dinendra Raychaudhuri, On the Mimela Kirby, 1823 (Rutelinae: Scarabaeidae) of Buxa Tiger Reserve (a forest under biodiversity hot spot zone), Dooars, West Bengal, India. World Scientific News 50 (2016) 95-105
[27] Subhankar Kumar Sarkar, Sumana Saha, Dinendra Raychaudhuri, Anomala Samouelle, 1819 (Rutelinae: Scarabaeidae) of Buxa Tiger Reserve, Dooars, West Bengal, India.
Part – I. World Scientific News 65 (2017) 94-122
[28] Subhankar Kumar Sarkar, Sumana Saha, Dinendra Raychaudhuri, Anomala Samouelle, 1819 (Rutelinae: Scarabaeidae) of Buxa Tiger Reserve, Dooars, West Bengal, India.
Part – II. World Scientific News 118 (2019) 17-32
[29] Chandra, K. & Gupta, D. 2012. Diversity and composition of Dung beetles (Scarabaeidae: Scarabaeinae and Aphodiinae) assemblages in Singhori Wildlife
Sanctuary, Raisen, Madhya Pradesh (India). Munis Entomology and Zoology, 7(2): 812- 827
[30] Chandra, K. and Gupta, D. 2013. Scarab beetles (Coleoptera: Scarabaeoidea) of
Barnawapara Wildlife Sanctuary, Chattisgarh, India. Journal of Threatened Taxa, 5(12):
4660-4671
[31] Dacke, A., Bell, T.A. Foster, J. J. Baird, E.J., Strube-Bloss, M.F., Byrne, M.J. and Jundi, B.el. 2019. Multimodal cue integration in the dung beetle compass. Proc Natl Acad Sci U S A, 116(28): 14248-14253. doi: 10.1073/pnas.1904308116
[32] Davis, A. J. 2000. Does reduced-impact logging help preserve biodiversity in tropical rainforests? A case study from Borneo using dung beetles (Coleoptera: Scarabaeoidea) as indicators. Environmental Entomology, 29: 467–475
[33] Davis, A. J., and Sutton, S.L. 1998. A dung beetle that feeds on fig: Implications for the measurement of species rarity. Journal of Tropical Ecology, 13: 759–766
[34] Davis, A. J., Holloway, J.D., Huijbregts, H., Krikken, J., Kirk-Spriggs, A.H. and Sutton, S.L. 2001.Dung beetles as indicators of change in the forests of northern Borneo.
Journal of Applied Ecology, 38: 593–616
[35] Davis, A. L. V., Scholtz, C. H. and Chown, S. L. 1999. Species turnover, community boundaries and biogeographical composition of dung beetle assemblages across an altitudinal gradient in South Africa. Journal of Biogeography, 26: 1039-1055 [36] Davis, A. L. V., C. H. Scholtz, and Philips, T. K. 2002. Historical biogeography of
scarabaeine dung beetles. Journal of Biogeography, 29: 1217–1256
[37] Desiere, M. 1973. Ecologie des Coléoptères coprophages. Annales de la Societe Royale Zoologique de Belgiue, 103: 135–145
[38] Dickinson, C.H. and Craig, G. 1990. Effects of water on the composition and release of nutrients from cow pats. New Phytologist, 115: 139-147.
[39] Escobar, F. 2000. Diversidad de coleopteroscoprofagos (Scarabaeidae: Scarabaeinae) en unmosaico de habitats en la Reserva Natural Nukak, Guiviare, Colombia. Acta
Zoologica Mexicana, 79: 103–121
[40] Estrada A. and Coates-Estrada R. 2002. Dung beetles in continuous forest, forest
fragments and in agricultural mosaic habitat island at Los Tuxtlas, Mexico. Biodiversity and Conservation 11: 1903–1918
[41] Favila, M., and Halffter, G. 1997. Indicator groups for measuring biodiversity. Acta Zoologica Mexicana, 72: 1–25
[42] Fay, H. A. C. and Doube, B.M. 1983. The effect of some coprophagous and predatory beetles on the survival of immature stages of the African buffalo fly, Hematobia thirouxi potans, in bovine dung. Zeitschrift Fur Angewandte Entomologie, Journal of Applied Entomology, 95(5): 460–466
[43] Feer, F. 1999. Effects of dung beetles (Scarabaeidae) on seeds dispersed by howler monkeys (Alouatta seniculus) in the French Guianan rain forest. Journal of Tropical Ecology, 15: 129–142
[44] Fincher, G. T. 1975. Dung beetles of Blackbeard Island (Coleoptera: Scarabaeidae). The Coleopterists Bulletin, 29(4): 319–320
[45] Fincher, G.T. 1981. The potential value of dung beetles in pasture ecosystems. Journal of the Georgia Entomological Society, 16(1): 316−333
[46] Fincher, G. T., Monson, W. G. and Burton, G. W. 1981. Effects of cattle feces rapidly buried by dung beetles on yield and quality of coastal Bermuda grass. Agronomy Journal, 73(5): 775–779
[47] Fincher, G. T., and Woodruff, R. E. 1979. Dung beetles of Cumberland Island, Georgia (Coleoptera: Scarabaeidae). The Coleopterists Bulletin, 33(1): 69–70
[48] Fincher, G. T., Blume, R. R., Hunter, J. S. and Beerwinkle, K. R. 1986. Seasonal distribution and diel flight activity of dung-feeding scarabs (Coleoptera, Scarabaeidae) in open and wooded pasture in east-central Texas. Southwestern Entomologist
Supplement, 10: 1–35
[49] Fiene, J. G., Connior, M. B., Androw, R., Baldwin, B. and McKay, T. 2011. Surveys of Arkansas dung beetles (Coleoptera: Scarabaeidae and Geotrupidae): Phenologies, mass occurrences, state and distributional records. The American Midland Naturalist, 165(2):
319–337.
[50] Floate, K. D., and Gill, B. D. 1998. Seasonal activity of dung beetles (Coleoptera:
Scarabaeidae) associated with cattle dung in southern Alberta and their geographic distribution in Canada. Canadian Entomologist, 130(2): 131–151
[51] Floate, K. D. and Kadiri, N. 2013. Dung beetles (Coleoptera: Scarabaeidae) associated with cattle dung on native grasslands of southern Alberta, Canada. The Canadian Entomologist, 145(06): 647–654
[52] Frank, K., Bruckner, A., Hilpert, A., Heethoff, M. and Bluthgen, N. 2017. Nutrient quality of vertebrate dung as a diet for dung beetles. Scientific Reports, 7(12141): 1-12 [53] Galante, E. and Cartagena, M.C. 1999. Comparison of Mediterranean Dung Beetles
(Coleoptera: Scarabaeoidea) in Cattle and Rabbit Dung. Environmental Entomology, Volume 28, Issue 3: 420–424. https://doi.org/10.1093/ee/28.3.420
[54] Gollan, J. R., Reid, C. A. M., Barnes, P. B. and Wilkie, L. 2011. The ratio of exotic-to- native dung beetles can indicate habitat quality in riparian restoration. Insect
Conservation and Diversity, 4(2): 123–131
[55] Gascon, C., Lovejoy, T. E., Bierregaard, J. R R.O., Malcolm, J. R., Stouffer, P.C., Vasconcelos, H. L., Laurence, W. F., Zimmerman, B., Tocher, M. and Borges, S. 1999.
Matrix habitat and species richness in tropical forest remnants. Biological Conservation, 91: 223-229
[56] Gaikwad, A. R. and Bhawane, G. P. 2016. Observation on life cycle and nesting behaviour of dung beetle Onthophagus catta (Fabricius). International Journal of Zoology Studies, 1(7): 09-13.
[57] Ge´nier, F., and Kohlmann. B. 2003. Revision of the Neotropical dung beetle genera Scatimus Erichson and Scatrichus gen. nov. (Coleoptera: Scarabaeidae, Scarabaeinae).
Fabreries, 28: 57–111
[58] Halffter, G. and Arellano, L. 2002. Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica, 34: 144-154
[59] Halffter, G. and Edmonds, W. D. 1982. The nesting behavior of dung beetles (Scarabaeinae): An ecological and evolutive approach. México D.F., Man and the Biosphere Program UNESCO, 177 pp.
[60] Halffter, G. and Matthews, E.G. 1966. The natural history of dung beetles of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae). Folia Entomologica Mexicana, 12/14: 1-312.
[61] Halffter, G., Favila, M. E. and Halffter, V. 1992. A comparative study of the structure of the scarab guild in Mexican tropical rain forest and derived ecosystems. Folia Entomologica Mexicana, 84: 131–156
[62] Halffter, G., Favila, M.E. and Arellano, L. 1995. Spatial distribution of three groups of coleoptera along an altitudinal transect in the Mexican transition zone and its
biogeographical implications. Elytron, 9: 151–185
[63] Halffter, G. and Favila, M. E. 1993. The Scarabaeidae (Insecta: Coleoptera) an animal group for analyzing, inventorying and monitoring biodiversity in tropical rainforest and modified landscapes. Biology International, 27: 15-21
[64] Hammer, O. 1941. Biological and ecological investigations on flies associated with pasturing cattle and their excrement. Vidensk. Meddel. Dansk Naturhist. Foren, 105:
143–393
[65] Hanski, I. 1982. Dynamics of regional distribution: the core and satellite species hypothesis. Oikos, 38: 210–221
[66] Hanski, I. 1989. Dung beetles. In Tropical rain forest ecosystems (eds. H. Leith and J.
A. Werner), Elsevier Publishers, Amsterdam, Holland: 489–511
[67] Hanski, I. and Cambefort, Y. 1991a. Spatial processes. In: I Hanski & Y. Cambefort (Eds.). Dung beetle ecology. Princeton University Press, Princeton: 283-304
[68] Hanski, I and Cambefort, Y. 1991b. Competition in dung beetles. In: Hanski, I. & Y.
Cambefort, Y. (Eds.). Dung beetle ecology. Princeton University Press, Princeton: 305- 329
[69] Hanski, I. and Koskela, H. 1979: Resource partitioning in six guilds of dung-inhabiting beetles (Coleoptera). Annals Entomologica Fennica, 45: 1–12
[70] Hanski, I. and Krikken, J. 1991. Dung beetles in tropical forests in south-east Asia. In: I.
Hanski, & Y. Cambefort, Y. (Eds.). Dung beetle ecology. Princeton University Press, Princeton, 179-197
[71] Hanski, I. and Niemela, J. 1990. Elevational distributions of dung and carrion beetles in northern Sulawesi, 145–152. In: Rain Forest Insects of Wallacea. W. J. Knight and J. D.
Holloway (Eds.). Royal Entomological Society, London.
[72] Harpootlian, P. J. 2001. Scarab Beetles (Coleoptera: Scarabaeidae) of South Carolina.
Clemson University Public Service Publication, Clemson, SC.
[73] Helgesen, R. G. and Post. R. L. 1967. Saprophagous Scarabaeidae (Coleoptera) of North Dakota. Available online at www.ndsu.edu/fileadmin/
entomology/Publications/007a.pdf (Accessed on 15.5.2019)
[74] Hill, C. J. 1996. Habitat specificity and food preferences of an assemblage of tropical Australian dung beetles. Journal of Tropical Ecology, 12: 449–460
[75] Holter, P. 2004: Dung feeding in hydrophilid, geotrupid and scarabaeid beetles:
Examples of parallel evolution. European Journal of Entomology, 101: 365–372 [76] Horgan, F. G. 2005. Effects of deforestation on diversity, biomass and function of dung
beetles on the eastern slope of the Peruvian Andes. Forest Ecology and Management, 216: 117–133
[77] Howden, H. F. and Nealis, V. G. 1975. Effects of clearing in a tropical rain forest on the composition of the coprophagous scarab beetle fauna (Coleoptera). Biotropica, 7: 77–83 [78] Howden, H. and Howden, A. 2001. Change Through Time: a Third Survey of the
Scarabaeinae (Coleoptera: Scarabaeidae) at Welder Wildlife Refuge. The Coleopterists Bulletin, 55 (3): 356-362
[79] Howden, H. F. and Scholtz, C. H. 1986. Changes in a Texas dung beetle community between 1975 and 1985 (Coleoptera: Scarabaeidae, Scarabaeinae). The Coleopterists Bulletin, 40(4): 313–316
[80] Ishikawa, H. 2011. Effects of dung beetles on seedling emergence from herbaceous seeds in the dung of sika deer (Cervus nippon) in a temperate Japanese grassland ecosystem. Ecological Research, 26(4): 725-734
[81] Jadhav, M.J. and Sharma, R.M. 2012. Insecta: Coleoptera: Scarabaeidae: Scaeabaeid beetles. Fauna of Maharashtra, State Fauna Series 20 (Part-2), Zoological Survey of India, Kolkata: 489-494.
[82] Jankielsohn, A., Scholtz, C. H. and Louw, S. V. D. M. 2001. Effect of habitat transformation on dung beetle assemblages: A comparison between a South African nature reserve and neighbouring farms. Environmental Entomology, 30: 474–483 [83] Kadiri, N., Lumaret, J. P. and Floate, K. D. 2014. Functional diversity and seasonal
activity of dung beetles (Coleoptera: Scarabaeoidea) on native grasslands in southern Alberta, Canada. The Canadian Entomologist, 146 (3), 291–305
[84] Kalawate, A.S. 2018. A preliminary study on the dung beetles of the northern Western Ghats, Maharashtra, India. Journal of Threatened Taxa, 10(2): 11316-11331
[85] Kaufman, P. E. and Wood, L. A. 2012. Indigenous and exotic dung beetles (Coleoptera:
Scarabaeidae and Geotrupidae) collected in Florida cattle pastures. Annals of the Entomological Society of America, 105(2): 225–231
[86] Kessler, H., Balsbaugh, E. U. J. and McDaniel, B.1974. Faunistic comparison of adult coleoptera recovered from cattle and sheep manure in east central South Dakota.
Entomological News, 85: 67–71
[87] Kirk, A. A. 1992. The effect of the dung pad fauna on the emergence of Musca
tempestiva (Dipt, Muscidae) from dung pads in southern France. Entomophaga, 37(4):
507–514
[88] Klein, B. C.1987. Effects of forest fragmentation on dung and carrion beetle communities in central Amazonia. Ecology, 70: 1715-1725
[89] Klein, B.1989. Effects of forest fragmentation on dung and carrion beetle communities in central Amazonia. Ecology, 70: 1715–1725
[90] Koskela, H. 1972: Habitat selection of dung-inhabiting Staphylinids (Coleoptera) in relation to age of the dung. Annales Zoologici Fennici, 9: 156–171
[91] Koskela, H. and Hanski, I. 1977. Structure and succession in a beetle community inhabiting cow dung. Annales Zoologici Fennici, 14: 204-223
[92] Korasaki, V., Lopes, J., Brown, G. and Louzada, J. 2013. Using dung beetles to evaluate the effects of urbanization on Atlantic Forest biodiversity. Insect Science, 20(3): 393–
406
[93] Krantz, G.W. 1983. Mites as biological control agents for dung-breeding flies, with special reference to the Macrochelidae. In: Biological Control of Pests by Mites (Eds.
M.A. Hoy, G.L. Cunningham & L. Knutson), University of California, Berkeley, pp.
91-98.
[94] Krüger, K. and Scholtz, C. H. 1997. Possible risk posed by drift of the insect growth regulator pyriproxyfen to the rare dung beetle Circellium bacchus (F.) in a national park. Journal of insect Conservation, 1: 215–220
[95] Kudavidanage, E.P. and Lekamge, D. 2012. A provisional checklist of dung beetles (Coleoptera; Scarabaeidae) in Sri Lanka, pp.438-444. In The National Red List 2012 of Sri Lanka; Conservation Status of the Fauna and Flora (Eds. D.K. Weerakoon and S.
Wijesundara). Ministry of Environment, Colombo, Sri Lanka.
[96] Landin, B.O. 1961. Ecological studies on dung-beetles (Col.Scarabaeidae). Opuscula Entomologica Supplement, 19: 1–227
[97] Levesque, C. and Levesque, G. Y. 1995. Abundance and flight activity of some
Histeridae, Hydrophilidae and Scarabaeidae (Coleoptera) in southern Quebec, Canada.
Great Lakes Entomologist, 28(1): 71–80
[98] Liu, R. T., Zhao, H. L. and Zhao, X. Y. 2012. Influence of grazing exclusion on soil macroinvertebrate diversity in degraded sandy grassland (Inner Mongolia, China).
Polish Journal of Ecology, 60(2): 375–385
[99] Lobo, J. M., Martín-Piera, F. and Veiga, C. M. 1988. Las trampas pitfall con sebo, sus posibilidades en el estudio de lascomunidadescoprófagas de Scarabaeoidea (Col.). I.
Características determinantes de sucapacidad de captura. Revue d`ècologie et de biologie du sol, 25: 77-100
[100] Lobo, J. M., Lumaret, J. P. and Jay-Robert, P. 1998. Sampling dung beetles in the French Mediterranean area: effects of abiotic factors and farm practices. Pedobiologia, 42: 252–266
[101] Lobo, J. M., Lumaret, J. P. and Jay-Robert, P. 2001. Diversity, distinctiveness and conservation status of the Mediterranean coastal dung beetle assemblage in the Regional Natural Park of the Camargue (France). Diversity and Distributions, 7: 257–270
[102] Matheson, M. M. 1987. Insects associated with cattle dung in southern Québec. M.Sc.
thesis, McGill University, Montreal, Canada.
[103] Masan, P. and Halliday, B. 2009. Mesostigmatid mites associated with the dung beetle Copris lunaris (Coleoptera: Scarabaeidae). European Journal of Entomology, 106: 545–
550
[104] McGeoch, M.A., Rensburg, B.J.V, and Botes, A. 2002.The verification and application of bioindicators: a case study of dung beetles in a savanna ecosystem. Journal of Applied Ecology, 39: 661-672
[105] Medina, C. A., Escobar, F. and Kattan, G.H. 2002. Diversity and habitat use of dung beetles in a restored Andean landscape. Biotropica, 34(1): 181-187
[106] Menendez, R., and D. Gutierrez. 2004. Shifts in habitat associations of dung beetles in northern Spain: Climate change implications. Ecoscience, 11(3): 329–337
[107] Miranda, C. H. B., Dos Santos, J. C. C. and Bianchin, I. 1998. Contribution of
Onthophagus gazella to soil fertility improvement by bovine fecal mass incorporation into the soil. Greenhouse studies. Revista Brasileira De Zootecnia - Brazilian Journal of Animal Science, 27 (4): 681–685
[108] Moczek, A.P. and Niijhout, H.F. 2003. Rapid evolution of a polyphenic threshold.
Evolution & Development, 5: 259-268
[109] Montes de Oca E. 2001. Escarabajos coprófagos de un escenario ganadero típico de la región de los Tuxtlas, Veracruz, México: importancia del paisaje en la composición de un gremio functional. Acta Zool. Mex. (n.s.) 82: 111-132 (2001)
[110] Newton, P.N. and Malcolm, J.C. 1985. Dung and dung beetles in Kanha Tiger Reserve, Central Indian Highlands. Journal Bombay Natural History Society, 85: 218-220 [111] Nichols, E., Spector, S., Louzada, J., Larsen, T., Amezquita S. and Favila, M. E. 2008.
Ecological functions and ecosystem services provided by Scarabaeinae dung beetles.
Biological Conservation, 141: 1461-1474
[112] Nealis, V. G. 1977. Habitat associations and community analysis of south Texas dung beetles (Coleoptera: Scarabaeinae). Canadian Journal of Zoology, 5: 138-147
[113] Nummelin, M. and Hanski, I. 1989. Dung beetles of the Kibale Forest, Uganda: a comparison between virgin and managed forests. Journal of Tropical Ecology, 5: 349–
352
[114] Numa, C., Verdu, J. R., Rueda, and Galante, E. 2012. Comparing dung beetle species assemblages between protected areas and adjacent pasturelands in a Mediterranean savanna landscape. Rangeland Ecology & Management, 65(2): 137–143
[115] O’Hea, N. M., Kirwan, L. and Finn, J. A. 2010. Experimental mixtures of dung fauna affect dung decomposition through complex effects of species interactions. Oikos, 119(7): 1081–1088
[116] Olechowicz, E. 1974. Analysis of a sheep pasture ecosystem in the Pienieny mountains (the Carpathians). Ekologia Polska, 22: 589–616
[117] Olechowicz E. 1976. The role of coprophagous dipterans in a mountain pasture ecosystem. Ekologia Polska, 24: 125–165
[118] Pakaluk, J., Slipinski, S. A. and Crowson, R. A.1995. Biology, Phylogeny, and
Classification of Coleoptera: Papers Celebrating the 80th Birthday of Roy A. Crowson.
Muzeum i Instytut Zoologii PAN, Warszawa, Poland.
[119] Pimsler, M. L. 2007. A survey of the dung beetles in cattle manure on pastures of an organic and a conventional dairy farm in New York State. Honors Thesis, Cornell University, Ithaca, NY.
[120] Price, D. L. 2004. Notes on the Scarabaeoid dung beetles (Coleoptera: Scarabaeidae, Geotrupidae, and Trogidae) of Hutcheson Memorial Forest. New Jersey Entomological News, 117: 347–350
[121] Price, D. L., Brenneman, L. M. and Johnston, R. E. 2012. Dung beetle (Coleoptera:
Scarabaeidae and Geotrupidae) communities of eastern Maryland. Proceedings of the Entomological Society of Washington, 114(1): 142–151.
[122] Priyadarsanan, D.R. 2006. Insecta: Coleoptera: Scarabaeoidea: Scarabaeidae (Dung beetles), pp 91-135. Thirumalai, G. & E. Krishnan (Eds.). Fauna of Biligiri
Rangaswamy Temple Wildlife Sanctuary, Conservation Area Series 27, Zoological Survey of India, 263 pp.
[123] Psarev, A. M. 2002. Succession in an insect community inhabiting horse dung. Russian Entomological Journal, 11: 287–290
[124] Putman, R. J.1983. Carrion and Dung: The decomposition of animal waste, Studies in Biology, 156, Institute of Biology, London, UK: 62.
[125] Qie, L., Lee, T. M., Sodhi, N. S. and Lim. S. L. H. 2011. Dung beetle assemblages on tropical landbridge islands: small island effect and vulnerable species. Journal of Biogeography, 38(4): 792–804
[126] Quintero, I. and Roslin, T. 2005. Rapid recovery of dung beetle communities following habitat fragmentation in central Amazonia. Ecology, 12: 3303–3311
[127] Ratcliffe, B. C., and Jameson, M. L. 2005. Generic guide to New World scarab beetles.Availablefrom:museum.unl.edu/research/entomology/Guide/Guide- introduction/Guideintro.html (Accessed on 15.12.2020)
[128] Ratcliffe, B. C., and Jameson, M.L. 2013. Generic guide to New World scarab beetles.
Availablefrom:museum.unl.edu/research/entomology/Guide/Guideintroduction/Guidein tro.html (Accessed on 15.12.2020)
[129] Radtke, M.G., Carlton, C. E. G., Williamson, B. 2008. A Dung Beetle Assemblage in an Urban Park in Louisiana. Southeastern Naturalist, 7 (1): 101-110
[130] Raychaudhuri, D. and Saha, S. (Eds.) 2014. Atlas of Insects and Spiders of BuxaTiger Reserve. Publ. West Bengal Biodiversity Board and Nature Books India, Kolkata: 357 pp.
