Dung , their Mating Habits, and their Effect on the Environment

Emily Chaskey [email protected] BI507

Introduction

Dung beetles, although not one of the favorite of many people, may perform essential services to the environment in many ecosystems. Their gathering, transportation, and burying of the dung of various omnivores and herbivores helps to remove accumulations of manure, fertilize the surrounding areas, aerate the ground, and to disperse various seed types.

The term “dung beetles” typically refers to beetles belonging to the order

Coleoptera, Families and Geotrupidae, and subfamilies and

Aphodiinae. There are three main types of dung beetles: rollers, tunnellers, and dwellers. As the names suggest, rollers roll dung into balls, roll it away, bury it, and use it for food or egg- laying; tunnellers bury the dung near to where it originally lies for the same uses as rollers; and dwellers simply live in the dung pats. The front legs of most dung beetles have serrated edges for use in digging in dung and for digging holes in the soil. Female beetles typically have shorter back legs, while the males have long back legs for use in rolling dung balls along the ground. Also, the age of the beetles can be estimated by the serrations on the front legs, since they are worn down through a lifetime of digging and rolling.

Adult beetles are drawn to manure by the odor, and some species will fly up to ten miles in search of the right patch of dung. Adult dung beetles use only the liquid contents of the manure for their nutrients; they do not actually “eat” the dung. Dung larvae eat the dung brood balls that they are laid inside. After hatching, the larva eats 40 to 50% of the

1 dung contained in the ball, and then pupates inside the brood ball as well. After the young

adult beetle emerges, it eats its way out of the brood ball, tunnels to the surface, and starts

the cycle over again.

One benefit from the relocation and burying of herbivore and omnivore dung is a

re-introduction of nutrients to the soil. This raises the general quality of the soil, and can

lead to a significant increase in the growth and health of pastureland plant species. The

aeration of the soil by burrowing beetles also increases the soil’s ability to absorb and hold

water. These improvements make the land more efficient for cattle grazing. Another

benefit is simply the removal of the feces from the pastures. Cattle benefit from the

reduction in fly populations and recycled gut parasites. Removal also helps with

contamination of the grazing area, allowing more cattle to feed.

Variations in Species

Different species of dung beetles have varied feeding patterns and preferences (fresh

vs. old dung, nocturnal vs. diurnal, etc). For example: Aphodius granarius and Aphodius erraticus are present in North Carolina from late winter through spring, but are not common during summer and fall; Phaenus vindex are found spring to fall; many Onthophagus species,

including O. hecate and O. taurus, are present starting in late March and are most active

through October. Dung beetles also have predilections for distinct climates, from arid

desert-like conditions to humid forests (Thomas, 2001). In addition to variations in seasonal

abundance and location, there are distinctions even between the times of day these beetles

feed, with many being nocturnal and relying on the polarization of moonlight to navigate

(Dacke, et al., 361-365). Many experts are now advocating the introduction of foreign

species to cattle ranges. This diversification would increase the dung beetle population

2 overall, and, through careful planning, could also give us a continual cycle of dung removal.

A continual cycle of dung removal could be the key to ensuring that our pastures are more

desirable for the cattle grazing in them, and could increase the usability of these pastures and

the production levels of our livestock.

Mating Behavior

Many dung beetle species have dimorphic males. These males are divided into major

and minor morphs, where major males have large horns, and minor males have very short

horns, or no horns at all. Oddly enough, the differences in horn length, while not due

directly to parental genetics, are due to the parents of the beetles, as will be explained.

Major and minor dung beetle males have significantly different behaviors in courtship, mating, and postcopulatory behavior (mostly parental provisioning). In

Onthophagus males, all males show distinctive “upward jerks of the head and pronotum” when initiating courtship with a female dung beetle. During this behavior, major males are more likely to be in direct contact with the female beetle than minor males (82% versus

56%), and were also more likely to contact the female head on (78% versus 39%). This has a negative impact on the number of times the major males get to breed, as it appears to visibly shake the females, to the point of pushing them backward. In a study by Cook (1990), 97% of hornless males initiated courtship behavior, compared to 82% of horned males.

However, while 61% of the hornless males were successful in inseminating the female, only

13% of horned males successfully mated.

Although this would seem to be a notch in favor of the hornless males and their ability to produce offspring, this may not be the case. Horned males are much more likely to cooperate with the females they mate with after copulation. In O. bindis, this amounted to

3 ten occasions of cooperation between a female and a large male, while hornless males were never seen cooperating with their mates (Cook, 1990). Horned males are involved in moving the dung to the burrow entrance and then passing it down into the burrow, as well as sometimes gathering the dung. This involvement is actually positively correlated (Hunt and Simmons, 2002). Males and females do not act alone. Rather, they cooperate with one another, filling in the gaps in parental care that the other may have left. This cooperation is also vital to the weight of the brood masses, as a male and female together are able to compile a larger amount of dung before the eggs are laid.

Cook (1990) also hypothesized that the horned males mate less often on purpose.

“By lifting and shaking the female during courtship, the horned male may acquire information on the female’s size or body weight. Males might choose females on the basis of size since size is positively correlated with fecundity in female O. bindis as in the dung beetle Copris diversus.” This discrimination toward potential mates would also help account for the larger size of the brood masses and potential offspring. In contrast, minor males have actually been known to dig holes along side of the holes being guarded by horned males in an attempt to mate with the female that is already preparing to lay eggs in a brood ball. This behavior alone shows that hornless males are indiscriminate in their choice of a mate.

O. bindis females produced more offspring when paired with horned major males than when they pair with minor, hornless males (Cook, 1990). In other studies, such as those by Kotiaho (2002), it was shown that species such as O. taurus produce larger offspring when they mate with the larger horned males than when they mate with hornless males.

This is probably a result of the involvement of the major males in the production of brood balls and the guarding of the nests, giving their offspring more nutrients and protection from

4 competing dung beetles and other predators. This phenomenon, where females mated with large males provide more resources to their offspring, has actually been termed the “mother- in-law effect” by Hunt and Brooks (2002). The lighter brood masses (less offspring) produced in O. taurus by mating with large males leads to the production, therefore, of larger offspring from the same amount of initial investment of dung. These larger offspring are, in turn, able to better provide for their offspring, continuing the cycle.

Dimorphism in male horn lengths is a result of parental care rather than the genetics of the parents of the larva. The amount of nutrients provided for a larva in the initial brood ball is an accurate indicator of whether or not the resulting male offspring will have horns or not (Moczek 1998, Moczek 1999, Hunt and Simmons 2000, Hunt and Simmons 1998).

Once male O. taurus larvae reach a body size of 5 mm protonum width, they change from investing in body size to investing to the production of horns (Hunt and Simmons, 2000). If there are enough nutrients in the brood ball to support both growth to that size, and development of a horn, the larvae will develop into a major male, and will generally be large as well. Therefore, the involvement of the male in production and protection of the larva provides significant pushes toward the development of a large major male. Even though the horned phenotype is not genetically passed down, it is still more likely that the progeny of a horned male will have horns than the progeny of a minor male.

The use of major males in breeding and addition of dung beetles to stock land would be advantageous. Females that mate with major males can produce either larger offspring or more offspring. Both results would lead to a greater use of dung piles, as larger offspring and larger brood sizes would require a larger initial stock of food, and would require more dung throughout their lifetimes. This advantage would be passed down from generation to generation, as the large offspring had large offspring, and so on.

5

Effects on the Environment

Dung beetle activity in pastures plays a great role in the number of parasites acquired by cattle, as well as reducing the fly population and improving the soil quality. The burial of feces that contains parasite eggs decreases the ability of those parasites, once they have hatched and reached the infective stage, to actively infect livestock (Fincher, 1975). Parasite free calves were placed in pastures “contaminated” with parasitic helminth larvae, but with different numbers of dung beetles. Pasture B constantly had dung beetles removed and placed into pasture A, while pasture C was untouched, except to contaminate it with parasites. Consequently, pasture A had 2 times more dung beetles than pasture C, and 10 times more dung beetles than pasture B throughout the study. Calves in pasture B had 9 times more parasites than calves in pasture A, and 2.3 times more parasites than calves on pasture C. As can be seen, the number of parasites acquired by calves was very closely negatively correlated to the number of dung beetles in the pastures. These effects are corroborated by Bryan (1976) through his study introducing pairs of Onthophagus gazelle to pastures containing cattle infected with nematodes. He found that in dung pats attacked by two, 10, and 30 pairs of beetles, the number of larvae surrounding the dung pat was reduced by 40, 74, and 66 percent, respectively, in comparison to control pats not exposed to beetles.

These two studies, although older, show that the addition of dung beetles can significantly reduce the number of harmful parasites found in contaminated pastures.

Burial of dung by Onitis species significantly reduced the number of fly larvae that survived in the dung (Edwards and Aschenborn, 1978). Due to the short development period of bushflies and buffalo flies (6 days), burial of dung within the first 6 days after it is dropped is most effective. In the Onitis genus of dung beetles alone, there are five species

6 that meet this requirement: O. uncinatus, O. caffer, O. alexix, O. pecuarius, and O. aygulus.

Through the thousands of species of dung beetles world wide, there are bound to be many

more that would fill the specific niche of fly larvae control.

Burial of dung can have considerable effects on the nutrition in pasture soil. Dung

beetle activity in various environments, including clay, loam, and sand, have been shown to

significantly increase the concentration of primary nutrients such as phosphorus and

potassium, secondary nutrients such as calcium, magnesium, and sulfur, and micronutrients

such as zinc, manganese, and copper. In addition to helping re-invest these important

nutrients, dung burial helps raise the soil pH in sandy soils. Interestingly, dung burial also

increases the cation exchange capacity (CEC) in all three soil types. This means that not

only do the dung beetles add extra nutrients to the soil, they also increase the ability of the soils to hold the basic cations in these nutrients (Calcium, Potassium, Magnesium) (Bertone et al. 2006).

Obviously, the quantity of dung buried and shredded by dung beetles is correlated to the biomass of the beetles in the pasture or pad (Tyndale-Biscoe, 1994). However, some species of beetles bury more quickly or more often than others. For example, one pair of

Onitis caffer buried 789 G of dung in 12 days, while a pair of O. uncinatus buried only 155g in

the first days. Also, O. caffer and O. aygulus start to bury dung immediately after being added

to a patch, while other beetles such as O. viridulus did not start burying at a rapid rate until 6

to 9 days had elapsed. These variations, while problematic in the prevention of parasitic

larval growth, are good news for the removal of dung. Beetles that will consume fresh dung

can only remove so much before the pat dries out and is no longer appetizing. The presence

of beetles that start to use the dung pat when it is old are helpful in the complete removal of

livestock manure.

7 Conclusions

Dung beetles are much more complicated than they appear at first glance. The ancient Egyptians thought that dung beetles were all males, and created progeny spontaneously by injecting semen into balls of dung. Although this is not true, it is an example of how much more complex life is than what we assume. The vast variation in mating behavior, feeding preferences, habitat choices, and seasonal abundances in dung beetles lend them to being the perfect choice for modification of pasture lands and improvement of all types of soil. Careful consideration would generally need to be given to the types of beetles used in these ventures, but even the addition of native beetles would dramatically increase the removal of livestock dung and the productivity of our soil. Further research into dung beetles and their life cycles will no doubt give us more understanding of how nature itself, through careful application, can be used for improvement and treatment of overcrowding and overuse of our lands.

8 Works cited

1. Bertone, M., et al. Dung Beetles of Central and Eastern North Carolina Cattle Pastures.

North Carolina Cooperative Extension. April 1, 2007.

http://graham.ces.ncsu.edu/depts/ent/notes/forage/guidetoncdungbeetles.pdf

2. Bertone, M., et al. The Contribution of Tunneling Dung Beetles to Pasture Soil

Nutrition. Plant Management Network. 11 July 2006.

3. Bryan, R. The effect of the Dung Beetle, Onthophagus gazelle, on the Ecology of the

Infective Larvae of Gastrointestinal Nematodes of Cattle. Aust. J. Agric. Res. 27 (1976):

567-574.

4. Cook, D. Differences in courtship, mating and postcopulatory behaviour between male

morphs of the dung beetle Onthophagus binodis Thunberg (Coleoptera: Scarabaeidae).

Anim. Behav. 40 (1990):428-436.

5. Dacke, M., et. al. Lunar orientation in a beetle. Proc. Biol. Sci. 271 (2004):631-635.

6. Edwards, P., Aschenborn, H. Patterns of nesting and dung burial in Onitis dung beetles:

Implications for pasture productivity and fly control. Journal of Applied Ecology 24

(1987): 837-851.

7. Emlen, D., Philips, T. Phylogenic Evidence for an Association Between Tunneling

Behavior and the Evolution of Horns in Dung Beetles (Coleoptera: Scarabaeidae:

Scarabaeinae). Coleopterists Society Monograph, 5 (2006): 47-56.

8. Fincher, G. Effects of dung beetle activity on the number of nematode parasites

acquired by grazing cattle. The Journal of Parasitology Vol, 61 No. 4 (1975): 759-762.

9. Hunt, J., Brooks, R. The mother-in-law effect. Proc. R. Soc. Lond. 271 (2004): S61-S63.

10. Hunt, J., Simmons, L. Behavioural dynamics of biparental care in the dung beetle

Onthophagus taurus. Behaviour, 64 (2002(a)): 65-75.

9 11. Hunt, J., Simmons, L. Maternal and Paternal effects on offspring phenotype in the dung

beetle Onthophagus taurus. Evolution, 54 (2000): 936-941.

12. Hunt, J., Simmons, L. Patterns of parental provisioning covary with male morphology in

a horned beetle (Onthophagus taurus) (Coleoptera: Scarabaeidae). Behav. Ecol. Sociobiol.

42 (1998): 447-451.

13. Hunt, J., Simmons, L. The genetics of maternal care: Direct and indirect genetic effects

on phenotype in the dung beetle Onthophagus taurus. PNAS Vol. 99, No. 10 (2002(b)):

6828-6832.

14. Kotiaho, J. Sexual selection and condition dependence of courtship display in three

species of horned dung beetles. Behavioral Ecology Vol. 13 No. 6: 791-799.

15. Moczek, A. Facultative paternal investment in the polyphonic beetle Onthophagus taurus:

the role of male morphology and social context. Behavioral Ecology Vol. 10, No. 6

(1999): 641-647.

16. Moczek, A. Horn polyphenism in the beetle Onthophagus taurus: larval diet quality and

plasticity in parental investment determine adult body size and male horn morphology.

Behavioral Ecology Vol. 9, No. 6 (1998): 636-641.

17. Ocampo, F., Philips, T. Food relocation and nestinbg behavior of the Argentinian dung

beetle genus Eucranium and comparison with the southwest African Scarabaeus (Pachysoma)

(Coleoptera: Scarabaeidae: Scarabaeinae). Rev. Soc. Entomol. Argent. 64 (2005): 53-59.

18. Palestrini, C., Rolando, A. Body size and paternal investment in the genus Onthophagus

(Coleoptera, ). J. Zool., Lond. 255 (2001): 405-412.

19. Sato, H. Male participation in Nest Building in the Dung Beetle Scarabaeus catenatus

(Coleoptera: Scarabaeidae): Mating Effort Versus Paternal Effort. Journal of

Behavior, Vol. 11, No. 6. (1998).

10 20. Sato, H. Two nesting behaviours and life history of a subsocial African dung-rolling

beetle, Scarabaeus catenatus (Coleoptera: Scarabaeidae). Journal of Natural History 31

(1997): 457-469.

21. Thomas, M. Dung Beetle Benefits in the Pasture Ecosystem. Appropriate Technology

Transfer for Rural Areas. October 2001. http://attra.ncat.org/attra-

pub/dungbeetle.html

22. Tyndale-Biscoe, M. Dung Burial by Native and Introduced dung Beetles (Scarabaeidae).

Aust. J. Agric. Res., 45 (1994): 1799-1808.

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