Chapter 8. Mating behavior in Achatina fulica
Introduction
Mating in pulmonates generally means a simultaneous exchange of sperm between copulated individuals. Although there were many studies on mating behavior in many land snails in the past, our available knowledges on the mating behavior of A. fulica are quite poor. In this chapter, I investigated the mating behavior of A. fulica in detail. The subjects dealt with were included mating activity, courtship behavior, duration of copulation, repeating ability of copulation in an individual.
Materials and Methods
1. Observation site
Observations were made mainly in shrub and grass fields locating near D-site described in chapter 2.
2. Hourly change in number of copulating pairs.
The number of copulating pairs was counted by every 30 minute patrols during the period from 4:00 p.m. to 9:00 a.m. at the following 7 nights; 20 April, 22 June, 1988, 24 April, 25, 27, 28, and 29 June, 1989. The weather of these nights was fine and dry. Night observations were mad under red light, and the number of those pairs which were inserting penis each other was counted in the area of 2km@m along a road.
3. Observations on courtship behavior and duration of copulation.
In order to estimate the duration time of copulation, an another site other than the above mentioned one was chosen, and patrolled every 15 minute during the period from 4:00 p.m. to 9:00 a.m. The commencement of copulation means the finding time of a pair, and the end was the time at which that pair was found separately on the way of patrol. Each pair found was discriminated by numbered stakes set near respective pairs. At this time, shell length of paired individuals was measured for classifying them into the following two categories; subadult and adult. Such a night patrol was sporadically repeated in breeding seasons of 1987, 1988, and 1989. In several nights, whole mating processes were observed on many pairs, and every events happed was recorded for analyzing mating behavior.
4. Repeating ability of copulation in an individual.
Radio-tagged individuals were traced for 25 successive nights from 22 June to 15 July 1989 in D-site. Copulated individuals found were recorded together with the characteristics of mates, for example shell length and copulating position (upper and lower).
5. Characteristics of mates chosen in copulation.
In order to examine the characteristics of mates chosen in copulation, 210 pairs were collected from different places at different occasions in the breeding seasons in 1987, 1988, and 1989. At the time of collections, the shell length, copulating position, and other necessary characteristics of each pair were recorded, and all the pair collected were dissected in order to examine reproductive system after preservation in ethanol solution.
Results
1. Mating activity
Figure 31 shows hourly changes in number of copulating pairs observed in each 3 successive night in April and in June, 1989. During daytime, copulating pair was found only in small number. When night came, however, the number of copulating pairs increased rapidly and, after reached at a peak at midnight, decreased gradually toward the following morning. In other words, mating activity becomes intense sharply from just after sunset to midnight, but begins to decrease after midnight. Since copulation generally continued for several hours, the number of copulating pairs found at the time around midnight became most large. The difference in height of peaks at this time between the countings in April and in June in the graph is probably due to the seasonal difference in reproductive activities between both seasons.
The above mentioned hourly change in mating activity was also reconfirmed by Fig.32, which showed the frequency distribution of commencement time of copulations occurred during one night. According to the graph, copulation began to occur at 7:00 p.m., thereafter sharply increased in number by 10 p.m., and then followed a gradual decrease by 5:00 a.m. of the following morning. When we consider the pair combinations between subadult and adult, the copulations of adult-adult combination were observed only in the period from 7:30 p.m. to 12:30 p.m. Contrary, the copulations of subadult-subadult combination were observed at any time. These facts indicate that subadults are quite active throughout a night, while adults become active only in the period from 7:30 p.m. to 12:30 p.m.
2. Courtship behavior.
A whole process of courtship behavior in the field was observed on 223 pair in total. According to such a field observation, the process of courtship was able to divide into several distinct steps as described in Table 7.
Apparent courtship began at the time of close approach between two individuals. At the time of contact, a positive individual touched with its tentacles to the other which was still sedentary or slowly crawling and, when the former began to mount on, the latter started to react following the steps described in Table 7. In the most case, upper position (initiator to court) is subadults and lower position (receiver) is adults. If these steps described in Table 7 were completely satisfied by 2 individuals met, a successful copulation would be realized. The time required from mounting to peins insert was about 5 minutes. During copulation, several other individuals gathered at times and mounted on the copulating pair, thus the pair was generally fallen down horizontally. Since the individuals gathered never tried to court or extended their penis, the pair was able to conclude copulation.
When either of mates did not court following the above mentioned steps, copulation was sometimes failed. The failure of copulation occurred at the steps a, b, c, and d shown in Table 7. The failure generally occurred rejection by either of mates. Figure 33 shows the percentages of successful and failed copulations observed on 223 pairs. The rate of rejection by snails of upper position reached 75.3% (168 examples), while that by snails of lower position 13.9% (31 examples), thus the rate of success became only 10.8% (24 examples). Since the steps a, c, and d were satisfied by the reaction of lower-postioned snail against upper-positioned snail, it seemed that the lower-positioned snail mainly had its option on rejection to the courting mate at that time. Rejection by the upper- positioned snail occurred only when the step b was not satisfied by the lower-positioned snail.
Figure 34 shows the percentages of failed examples occurred at each courtship step. As shown in the graph, 65.5% (146 examples) of failure occurred at the time of mounting (step a). All these cases were resulted from rejection by lower-positioned snails. Of this percentages, 34.5% (77 examples) occurred by the case in which backward bending by lower-positioned snail (step b) was lacking. The percentage of failure due to the rejection by upper-positioned snail in spite of the existence of backward bending by the lower-postioned snail was 13.9% (31 examples).
Such mating failures due to behavioral disagreement between two individuals seem to have a close connection to the difference of body size between them. According to the observation on 210 mating pair arbitrary sampled in the breeding seasons of 1987 to 1989, the percentage of failure was sharply increased when the difference of shell length between mates became larger than 10 - 15mm (Fig.35). No successful copulation was observed when the difference of shell length between mates became longer than 21mm. In such a case of failure, large mate in shell length rejected the other small, thus courtship between them terminated at early step of the mating behavior.
3. Duration of copulation
Figure 36 shows the distribution of duration times required for a copulation. In the graph, each histogram was shown by dividing into 3 different pair combinations of subadult-subadult, subadult-adult, and adult- adult. A shown by the graph, the duration time of copulation varied greatly from pair to pair, and a mean duration time was calculated to be 4.58 hours. However, the duration time in the pair of adult-adult combination was significantly longer than that of the other combinations. In other words, subadults tend to finish copulation in shorter time than adults.
When we come to this point, there arises a question whether or not the duration time of copulation have an important relation to the sperm injection. In order to investigate this point, successfully copulated 76 pairs were collected, and the individuals copulated at lower-position were dissected for measuring the weight of bursa copulatrix. Figure 37. shows the result obtained. It is clear from the graph that the weight of bursa copulatrix was positively correlated with the duration time of copulation. Although there was a large variation, this tendency was common in different pair combinations between subadult and adult. Therefore, a long lasting copulation have an important meaning in this snail.
4. Repeating ability of copulation in an individual
According to the results obtained from the observations on the copulation of radio-tagged individuals, no individual copulated more than once during a night.
Figure 38 shows the copulation histories of 8 radio-tagged subadults and adults during the period of tracing for 25 successive nights. In the case of subadults, they repeated copulation with irregular intervals, or at times successively for 2 to 4 nights. Contrary, adults intermitted copulation with a pause of about 10 nights after they repeated 2 to 3 times in successive nights or every other night. In short, subadults tend to repeat copulations more frequently than adults. The 10 days pause observed in adults is probably the period during which they lay eggs. In addition, it was shown by the graph that subadults copulated in upper position to the mate, while adults generally took lower position. These fact means that subadults are apt to be initiators of courtship, but adults receivers.
Figure 39 shows the difference of mates copulated with radio-tagged subadults and adults in respective nights indicated in Fig. 8. As clearly shown by this graph, the mates chosen by the radio-tagged individuals during 25 days were largely adults. Although subadults sometimes chose subadults as their mates, but adults did rarely so. In other words, there is a tendency that both subadults and adults chose adults as preferable mates.
Discussion
In land snails, courtship generally last long time. It has been known that a rain bring about an increase of mating activity. In the present study, it was revealed that copulation of A. fulica occurred most frequently in the period from 10:00 p.m. to 3:00 a.m. in the following morning. In other wards, this animal is not crepuscuar but strong nocturnal. Subadults were active during whole nighttime, but adults tended to become active during the period from 8:30 p.m. to 12:30 p.m. Such a difference in copulatory activity has not been reported in other land snails.
The mating behavior of A. fulica involved several distinct steps as shown by Table 1. It seems that these steps of behavior are heritable, because every individuals followed these steps in the process of courtship. Courtship of pulmonates, especially of slugs, sometimes involves a turning dance drawing an everclosing circular path. In Deroceras sturany and some other slugs, it has been noted that only clockwise-direcyted circling gives successful copulations, because counterclockwise movement faced their genital pore to that of mate (Kosinska, 1980).
The duration of courtship in A. fulica lasts only about five minutes. However, duration of copulation is long, a mean was calculated to be 4.58 hours. The duration of copulation differs between subadult and adult, the duration of the former is much shorter than that in the latter. Such a difference of copulation time in relation to the age of snail has never been reported in the other land snails. In some species, for example Deroceras, copulation lasts only a few minutes, but in some others, such as Limax, continues for 34 hours or more. It is said, however, that sperm transfer itself requires only several minutes (Tompa, 1984). A spectacular example of mating is that of Limax maximus. This slug hangs in a pair by thick mucus ropes suspending from trees (Fischer, 1917; Chase, 1953; Langlois, 1965).
Each pair of A. fulica performs reciprocal exchange of sperm simtaneously. The mating behavior was considerably differed between upper- positioned snails, generally subadults, and lower-positioned snails, mostly adults. If mating behavior is carefully investigated, it is suspected that such differences found in A. fulica were also detectable in other species. Langlois (1965) described the existence of "male-behaving" individual and "female-behaving" one in a pair of Limax maximus. In the case of A. fulica, it is possible to call the upper-positioned snails of courtship as "male- behaving" individual and the lower-positioned snails as "female-behaving" one, when we follow the definition by Langlois.
Snails sometimes suffer injury from copulation by the use of sharp darts or biting with jaw or radula. The snail ventridens, for example, stabs mate with a dart and bites with its radula (Webb, 1948). In A. fulica, biting with jaw was observed, but it was an important step of courtship.
It was revealed by dissection that A. fulica does not from spermatophore. This point differs from most other member of pulmonates. In some helicarionids, Hesperarion, 10-20 spermatophore have been found in the bursa copulatrix of a single specimen (Tompa, 1984). Trigonochlamys innitratrix is very likely to transfer more than one spermatofore by one copulation (Likharev and Wiktor, 1980). When the bursa diverticulm is present in A. fulica, it will become a preferred site of spermatophore deposit.
In the present study, it was observed that about 90% of snails courted with the others were rejected by their mates. Such a high rejection rate of mating has not been reported in the other land snails. As described in the text, the lower-positioned snails in courtship process have its option on rejection to the mate at that time. This result suggests that A. fulica is highly sensitive in mate choice.