E. G. Matthews.
Observations on the Ball-Rolling Behavior of Canthon pilularius (L.) (Coleoptera, Scarabaeidae).
Psyche 70:75-93, 1963.

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OBSERVATIONS ON THE BALL-ROLLING BEHAVIOR OF CANTHON PILULARIIJS (L.)
(COLEOPTERA, SCARABAEIDAE)
BY ERIC G. MATTHEWS'
Department of Biology, University of Puerto Rico, Rio Piedras The present paper describes some aspects of the normal behavior of Canthon pilularius (L.) (C. laevis [Drury]) in the field and is the result of direct observations totalling about 57 hours, carried out in four field locations in Florida and Georgia in 1957 and 1961. The approach of this study is neither ethological nor ecological, but taxonomic. That is to say, certain aspects of the normal behavior of the scarab were investigated and quantified with a view to using them as taxonomic characters in comparison with other related species and genera. My data on other species of the genus Canthon are not yet complete enough to present an interspecific analysis of the behavior of this genus, but are adequate for an intergeneric comparison with European representatives of the ball-rolling genera Scarabaeus, Gym- nopleurus, and Sisyphus, which have been studied in detail by Ger- man investigators. Such a comparison is now in preparation by the author and will be published subsequently. Previous literature gives the outlines of the life history of C. pilularius (Lindquist, 1935 ; Cooper, 1938 ; Ritcher, I 94 j ; Miller, 1954), but there are no published observations describing the behavior sequences seen. Brief notes on the biology of about 25 other species of Canthon, sensu stricto, have been recorded in the literature (see von Lengerken, 1954, Pereira and Martinez, 1956, and Halffter, 19 59, for discussions).
This species is commonly known in the United States literature as Canthon laevis (Drury). However, it has been known for some time that this is not the correct name. In a recent revision of the genus (Halffter, 1961) there is a review of the reasons showing why the name pilularius Linnaeus, 1758, is most probably correctly attributed to this species. Furthermore, Lane ( 1950) shows that even the name hudsonias Forster, 177 I, has precedence over laev'ts Drury, I 773. 'The present investigation was supported in part by Postdoctoral Research Fellowship No. 12,061 of the National Institute of Mental Health, N.I.H., U. S. Public Health Service, while the author was at the Biological Labora- tories, Harvard University. Publication of this work was aided by a grant from The Society of the Sigma Xi and RESA Research Fund. Manuscript received by the editor September 12, 1962. Psirfir 70:7S-93 (1963). hup #psyche rnkluborgflCV70-075 html



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Acknowledgments
I wish to acknowledge the helpfulness shown by the University of Florida in general and Mr. William M. Dunson in particular in extending to me the facilities of the Welaka Reserve, on which some of this study was carried out. Mr. 0. L. Cartwi-ight of the United States National Museum made the authoritative determinations identifying the specimens involved. To Dr. Howard E. Evans of the Museum of Comparative Zoology and Dr. I?. M. Carpenter of the Biological Laboratories, Harvard University, I am particularly grateful for reading the manuscript and making many helpful suggestions.
Methods
The methods used consisted of sitting down and watching the activities of the scarabs after a quantity of human faeces or cow dung had been placed in a suitable location. Complete notes were taken describing the actions of the beetles involved, the rolling patterns were diagrammed in the field notebook, and pertinent data such as time in minutes, distances rolled (measured with a metric tape meas- ure), terrain features, wind direction, sun position, etc. were recorded. The author always camped in the immediate area of observation so that he could be present for every phase of activity from beginning to end. Often several days were spent in the same spot, and it need hardly be mentioned that every hour of observation represents many additional hours of waiting. No special techniques were used and no experimentation was attempted. Beetles were marked with dabs of clear nail polish mixed with oil paints in different color combina- tions for identification; these markings were found not to last for more than a day or so because of the burrowing activity of the beetles. The study was carried out near Arcadia, De Soto County, Florida, on 27 March, 1957, in the Osceola National Forest, Columbia County, Florida, on 7 - I T June, 1957, near Brunswick, Glynn Coun- ty, Georgia, on I 3 - 14 June, 1957, and near Welaka, Putnam Coun- ty, Florida, on 24 April - 6 May, 1961.
The illustrations (figs. I - 5) are traced exactly from ~hotographs taken by the author and may be considered completely accurate in regard to the positions and the attitudes of the beetles and the gen- eral size and shape of the balls.
Distribution and Color Phases
Canthon pilularius (L.) is widespread in the eastern half of the United States from extreme south-eastern Wyoming, Kansas, Okla- homa, and northern Texas eastward. It is replaced in most of Texas



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19631
Matthews - Behavior of Canthon
77
and the Southwest by the closely related C. imitator Brown, which also occurs in Oklahoma, Arkansas, Louisiana, and Florida. In northern Florida east of the Apalachicola River and in southern Georgia a green or bronze phase of pilularius largely replaces the usual black one, while in most of peninsular Florida the species is largely represented by a blue-black phase which becomes intensely blue in the Keys. A more extensive discussion of the color phases will be found in Halffter (1961). The present observations are on all three color phases - green or bronze, black, and blue-black - and several instances of sexual pairing between all possible color combinations were observed, supporting the taxonomic evidence that there are no specific differences between them.
Morphology
The beetles are large ( 10 - 19 mm in length), broadly oval, and somewhat flattened (figs. I - 5). The head and legs are used exten- sively in the behavior described below and should therefore be briefly described. The head is strongly flattened and broad, with sharp edges, and is an excellent digging tool. The fore tibiae are strongly flattened and provided with teeth on the outer edges. The forelegs are used
extensively in cutting and manipulating the dung and in patting the surface of the dung ball, as well as in digging. The middle and hind tibiae are very slender and a little curved and are used in rolling and guiding the dung ball. For a very detailed study of the mor- phology of the genus, see Halffter ( I 961 ) . The mouthparts have been described by several authors (Hai-den- berg, 1907 ; Mohr, 1930; Pel-eira and Martinez, 1956 ; Miller, 1961 ) and do not concern us here, particularly. The latter author showed that the molar surfaces of the mandibles are so constructed as to be capable of a very thorough grinding action. Beetles with a mandible removed were unable to feed.
There is no sexual dimorphism, other than in the forespur, and it is therefore not possible to determine the sex of a beetle without examining it closely. This complicates observation somewhat and means that a behavior sequence must be interrupted or allowed to be completed before the sex of the participants can be determined. This can be done by looking at the forespur (a lens is usually not necessary), which is bifurcate in the male and simply acute in the female.
Ecology
The autecology of this species has not been properly investigated (nor has that of any other American coprophage). It is common




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knowledge that the species feeds on cow dung in pastures, and my observations indicate that older dung is preferred. Decaying meat rarely attracts the beetles (Lindquist, 1935) and cadavers of small vertebrates may occasionally be made into balls and rolled off (Bragg, 1957~)) as is commonly seen in some South American species of the genus (Luederwaldt, I 9 I I ) . Human dung is readily taken, and many of the observations which follow are based on feeding behavior with human faeces.
Miller (1954) analysed the role of 17 species of coprophagous scarabs in the dispersal of human faeces in the same general geo- graphical area in which this study was carried out. He found that C. pil,ularius made up 64% of the scarabs collected at human fecal traps in an open field in the daytime and that this species, because of its size, is potentially capable of removing more than 90% of the total exposed human dung removed by scarabs in the daytime, or 61 % of the total at all times. This makes it by far the most important species of coprophage in this ecological situation (open fields). Tumble-bugs (Canthon, sensu lato) are not important in heavily overgrown situations, indicating the importance of the surrounding terrain.
The recent very fine studies of Landin ( 1961 ) on the ecology of Aphodiinae finally prove for this group what has long been suspected by students of the coprophages in general, namely, that it generally makes no difference what kind of dung is eaten by a given species, but only where it is deposited, that is, to what extent it will be affected by heat and desiccation. If the type of dung is important (as for instance in the cases of cow and horse dung), it is because its consistency or shape may influence temperature changes and evap- oration rates (Landin, op. cit.).
In C. pil~uZarius activity is at the highest level in the spring and is very much dependent on rains, the most intense activity being seen immediately after showers. Activity usually begins at about 0900 on warm days (when the shade temperature reaches about goå¡ by I 100) and terminates at about 1700. During dry spells the beetles remain continuously inside cow droppings under the crust and I have not seen them spending this time in the soil. No studies have been made regarding optimal temperature and humidity limits for this species. In the localities in which I observed this species the soil consisted Qragg's observations on the rolling of decaying tadpoles were apparently made in central Oklahoma and therefore perhaps on the closely related Canthon imitator Brown.




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19631 Matthews - Behavior of Canthon 79
entirely of white sand and was largely exposed, either on sand roads or open pastures.
Ball-rolling Behavior
The apparent function of the making and rolling of a ball of dung is to transport the dung away from the dropping and bury it to be eaten underground, where it is protected from desiccation. The dung ball serves as food either for the beetle rolling it or for the future larva. Reproductive activity is seen almost entirely during the spring months (March - May), after which adult feeding activi- ty predominates. The behavior sequence in relation to the ball is signifi- cantly different depending on whether the dung ball is to serve as adult or larval food.
In the following account, the making and rolling of the food ball will be dealt with first.
Quantitative or important statements are followed by a number in parentheses; this indicates the number of observations upon which the previous statement is based. This is to enable the reader to judge the relative reliability of a statement. Apparent discrepancies in these observation numbers are due to the fact that many fragmentary sequences were observed. Anthropo- morphisms must be excused by the reader in the interest of avoiding lengthy circumlocutions.
The Food Ball
With regard to the food ball, both sexes behave the same way, acting individually. The sequence involved in the making, rolling, and burial of the ball is as follows: I) Approaching the dung source, 2) cutting, 3) shaping, 4) rolling, and 5) burial of the ball. An additional section below is devoted to underground feeding. The approach. When there is a wind, the beetles will approach a source of dung from down-wind, flying very low in zig-zags. At a certain moment, perhaps when the odor currents are encountered at a certain frequency,
the beetle suddenly "cuts" its power and drops like a stone to the ground, often landing on its back. The point where it lands may be from three to 80 cm from the dung, usually 10 - I 5 cm (5). The beetle then approaches on foot, moving jerkily with antennae outstretched. One beetle was seen to approach entirely on foot and was first spotted 150 cm away. The time it took for individual beetles to locate a given source of (human) dung
after deposition varied from less than one minute to five hours and 30 min (23 ) . Conversely, a given source of dung took from less than one minute to one hour and ten minutes to be first discovered by this species, the average being 23 min (6). Of course, these figures



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19631 Matthews -Behavior of Canthon 8 I
depend a great deal on very variable factors such as the density and searching activity of the beetles and the amount of dung in a given area.
Cutting.
Once a beetle has come up to a source of dung it begins immediately to start cutting a ball from the nearest portion. This process involves climbing on the dung and cutting a circular groove with the head and forelegs, the beetle pivoting in a circle. The dung is bunched up under the beetle with the forelegs and quickly acquires a ball-like shape (fig. I).
When the bunched dung is of a certain
quantity, it is detached by reaching under and cutting the lump away at the base in a circle (fig. 3). At this point, if the quantity of dung in the lump is adequate, shaping begins. If it is not, the beetle, resting on the lump, reaches out with the forelegs and grasps small quantities of dung from the main pile (or sometimes from balls of other beetles) and adds them to the lump (fig. I). I do not know how the beetle estimates the quantity of dung in the lump. The process of cutting takes 2 - 14 min, averaging 8.7 ~nin ( 12 ) . Shaping. Once cut and detached, the crude lump is converted into a more or less perfect sphere. Before shaping, the detached lump may be rolled a short distance (3 - 30 cm) away from the main pile. The process of shaping involves patting the lump rapidly over and over with the underside of the fore tibiae acting alternately, with the beetle climbing over the surface of the ball (fig. 2) or lying to one side of it and rotating the ball slowly so that the entire surface is patted many times over. The head may also be used to trim lumps or fibers off the ball surface during this process. Occasionally, new material may be added to the ball during the shaping process also (2). For the food ball, the shaping process takes 2 - 7 min, averaging 4.2 min (15).
At this point the ball is made, the entire process (cutting and shaping) having taken I 2 - 20 min and averaged I 5. I min ( I 2). The food balls are often crude and not symmetrical, and measure I 5 - 23 (All figures drawn from photographs taken by the author) Fig. 1. Lone beetle adding more material to food ball during cutting process. Fig. 2. Lone beetle shaping food ball. Forelegs are used to pat surface of ball. Fig. 3. Male and female pair cutting brood ball. Beetle at right is severing ball at base. Fig. 4. Male and female pair shaping brood ball. Both beetles are going over surface of ball with forelegs. Fig. 5. Rolling completed brood ball. Male is below, pushing ball backwards over an obstacle. Female is above, balancing on moving ball. This relationship of the sexes during rolling: is invariable. Note smooth contours of completed brood ball.



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82 Psyche [June
mm across their short diameter and 17 - 30 mm across their long, averaging 19.8 X 22.9 mm ( 1 1 ) .
At one location (Brunswick, Ga.), I repeatedly noted a curious activity by eight of the 18 beetles observed. It occurred during the shaping process and involved rapidly rotating the ball in the sand, in a stationary position, for about two minutes with the result that the ball became coated with sand. As the ball acquires a sand coat on being rolled anyway, this observation cannot yet be explained. Rolling. Once shaped, the ball is quickly rolled in a direction away from the dropping. Rolling is performed with the beetle head- downward behind the ball, pushing backward against the ground with the forelegs and steadying the ball with the middle and hind legs. The middle legs alternate between the ground and the ball and the hind legs are always in contact with the ball, alternately pushing against its surface with walking movements. When an obstacle is encountered the beetle will always attempt to push the ball over it rather than go around it (fig. 5). Frequent falls and tumbles occur, as a result of which the beetle may temporarily lose the ball. If this happens, the ball is searched for on foot in random patterns by the beetle, antennae outstretched. The procedure before resuming rolling after a tumble is always the same: the beetle climbs on top of the ball and turns so as to come down on the side of the ball necessary to resume rolling in the same direction in which it was rolling im- mediately before the tumble. Occasionally (2), the beetle will pause seemingly without reason, climb on the ball, turn around in either direction, and descend to resume rolling. Once started in a given direction, the beetle will continue in this direction about half the time (13 of 23), although the actual course followed is quite zig-zag at best. The rest of the time there are pronounced changes in direction during rolling (enforced direction changes due to obstacles are not counted here). I have attempted to relate the direction in which a ball is first rolled away from the dropping to three possible environmental factors: the wind direction, the slope of the ground, and the position of the sun. In figures 6 - 10 I have indicated by dots the initial directions taken in relation to each of these three factors in turn, according to 70 observations on both food and brood balls in all localities. The number of dots indicates the number of times a ball was seen rolled at a given angle (to the nearest 45O) from the ~osition or direction of the environmental factor indicated.
Chi-square calculations were made on each of the diagrams to



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19631 Matthews - Behavior of Canthon 83
ascertain the probability that the distributions obtained might have resulted by chance. Four class intervals were used for this, correspond- ing to four directions rather than the eight shown in the diagrams, since the numbers are too small to give meaningful results for eight class intervals. The chi-square figures and corresponding probabilities for three degrees of freedom are indicated in each diagram. The diagrams and numbers may be interpreted as follows: If the distribution is significantly skewed when all observations are plotted in relation to the direction of one particular factor, we may expect that this factor overrides all others in governing the direction the ball is rolled. Such a factor is obviously the slope of the ground, the beetles rolling uphill (P=<.oo~) (fig. 8). Another strong factor appears to be the wind direction (balls rolled with the wind), but it is evidently not as overriding (P=.025 - .05) (fig. 6). When all observations are plotted in relation to the position of the sun, the resulting diagram is not very strongly skewed, having a relatively high probability of being a chance distribution (P=.05 - -10) (fig. 9). We may interpret this to mean that the sun position is the least influ- ential of the three factors analyzed.
In order to pinpoint more accurately the influence of a single factor it is better to subtract observations which were also under the influence of other factors. It was possible to plot the directions in relation to the wind where the ground was level (minus the ground slope factor) (fig. 7), but this did not reveal a more significant relationship, for some reason. To have subtracted the sun factor as well would have left too few observations. The situation with regard to the sun is quite different when we plot the observations obtained when the other factors played no part, that is, when there was no wind and the ground was quite flat. In these cases, the distribution is very significantly skewed, with 13 out of the 19 observations being either directly toward or directly away from the sun (fig. 10). The probability that this could have been brought about by chance is .005. It appears, therefore, that the sun is used in some way in guidance, providing more important factors do not intervene. More will be said on this matter in the discussion at the end of the paper.
The relation to the wind may be simply explained: the beetle approaches the dung from down-wind and therefore tends to work on the leeward side of the dropping. Once made, the ball is simply rolled away from the dropping, and this will automatically be more or less in the direction of the wind, other factors being equal. The



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Directions Rolled in Relation to Three Environmental wind
Factors wind
6. All observations * ' 7. Minus ground
(U PI slope factor
sun
8. All
observations
sun
å´t
10. Minus ground slop*
9. All observations
and wind factors
MATTHEWS - CANTHON




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19631 Matthews - Behavior of Canthon 85
tendency to uphill rolling may also be simply explained by the fact that it is difficult to roll a ball sideways or downward on a slope without losing control of it.
The length of time that a food ball is rolled before burial varies from two to 18 rnin and averages 9.5 min (16) (not "about an
hour or more" as Lindquist states), and the distance rolled depends a great deal on terrain, of course; a heavily grassed or littered area impedes the progress of the beetle. The distance from the dropping that the food ball is rolled before burial varies from 15 to 830 cm, averaging 267 cm (19). This is not the straight-line distance, but that actually travelled by the beetle, as measured by tracing a line on the ground behind the beetle and measuring each twist and turn. It is evident that almost any spot will do for burial and the beetle is not "seeking" an ideal spot. It is not clear what factors prompt the beetle to begin burial, as both the time and distance rolled are very variable.
Burial. When the time for burial has arrived the beetle will pause and dig a little in the soil under the ball. This is presumably to test the ground to see if it is suitable for burial. Usually ( 12 of 16), the very first spot tested is that where the ball is buried. Otherwise (4 of 16), one or two other spots are tested before the final burial place is chosen, the beetle resuming rolling after rejecting a spot. Burial takes place by pushing soil to the sides from under the ball in such a manner that the beetle sinks rapidly into the ground with the ball on top of it. The food ball is buried 1.5 - 4 cm below the surface, that is to say, at a very shallow depth (9). At Brunswick, Ga., where I measured soil temperatures at burial depth I found them to be only I - 9O C below the air temperature of 35O C (10). Feeding. What happened after the food ball was buried was not directly observed, but some idea of the underground activity could be gained by unearthing different balls and beetles at varying intervals after burial. Fourteen such balls were dug up at intervals of I :35 to 49:30 hrs after burial and indicated the following: The beetle may not begin to nibble at the ball up to 6:08 hrs after burial, but on the other hand it may have begun feeding at I :35 hrs or earlier. The EXPLANATION OF PLATE 8
Figs. 6-10 represent the directions in which balls were seen rolled in relation to three different environmental factors in all localities, to the nearest 45' angle.
Total of beetles observed is 70. Each dot represents one observation in the given direction. Chi-square and corresponding probability figures for three degrees of freedom are given in each diagram. Further discussion in text.




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86 Psyche [June
ball is entirely consumed in 26 - 30 hrs after burial. The beetle stays with the remains of the ball for some hours and sometime between 30 and 50 hrs it departs, leaving only coarse fibers and beetle excre- ment in the hole.
Feeding by adults is said to occur also directly on the dropping, without a ball having been previously made (Lindquist, 1935). I have not observed this in this species in the field, although this habit is common in a related species (C, chalcites [Haldeman] ) . The Brood Ball
The behavior involved in the making and rolling of the ball destined to be converted into a brood pear3 and serve as. food for the larva is similar to that just described for the adult food ball but differs in a number of respects, the most important of which is the participation of both sexes in the making of a single ball. Although the importance of the male's role in this respect had been foreshadowed by comments in the literature on other species and genera (cf., e.g. Halffter, 1961, on C. h. humectus [Say] ) , I was surprised at the extent of the male's participation. The male plays the leading role in the making of the brood ball, and it is he exclusively who rolls, defends, and buries the ball, the female's role in these activities being purely passive. The following account will deal in turn with the encounter of the sexes, the making of the ball, rolling and burial, robbery and combat, and underground activity.
The encounter of the sexes. I was able to observe the crucial mo-