Semilunar courtship rhythm of the fiddler crab Uca lactea in a habitat with great tidal variation
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- Kim, T.W., Kim, K.W., Srygley, R.B. et al. J Ethol (2004) 22: 63. doi:10.1007/s10164-003-0100-4
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Semilunar courtship rhythm is a widely distributed phenomenon among fiddler crabs in the genus Uca (Decapoda, Ocypodidae). Typically, synchronous courtship has been reported to peak near spring tides. To determine whether a region of large tidal variation shifts reproductive activity, we measured the frequency of specific courtship behaviors including claw-waving and semidome building for U. lactea males on Kanghwa Island, Korea. We found that synchronized courtship for U. lactea peaked near neap tides, whereas near the spring tides, seawater flooded the habitat and males predominantly fed on the mudflat. Although active females, which hold their burrows and usually feed on the mudflat, are abundant near to spring tides, males rarely claw-waved to attract females. This pattern is atypical for the species because other populations of U. lactea on Japan and Taiwan are synchronous around spring tides. We suggest that males invest most of their time in feeding during spring tides because foraging is limited during neap tides. During neap tides, males feed infrequently and thus expend stored energy on courtship signals. We conclude that patterns of reproductive synchrony may be dependent on food availability in periodically changing environments.
KeywordsFiddler crabSemilunar rhythmSynchronous courtshipUca lacteaWaving
Many marine animals show reproductive rhythms following the semilunar or lunar tidal cycle (Palmer 1974; Ali 1992; Morgan and Christy 1994, 1995; Mizushima et al. 2000). Some fiddler crabs in the genus Uca are also known to have synchronous reproductive cycles (Christy 1978, 1986; Morgan and Christy 1994, 1995). Reproductive synchrony in fiddler crabs constitutes male courtship activity (Zucker 1978; Greenspan 1982; Salmon and Hyatt 1983; Salmon 1987), or the synchronous release of larvae from the female which follows the semilunar tidal rhythm (Christy 1978, 1982; Morgan and Christy 1994, 1995; Kellmeyer and Salmon 2001).
Previous studies of male courtship in fiddler crabs suggested that male courtship behavior is synchronized with female receptivity, which leads to simultaneous larval release (Christy 1978; Greenspan 1982; Salmon and Hyatt 1983; Salmon 1987). Coordinating this reproductive rhythm with the tidal cycle is assumed to be an adaptation that increases larval survival (Christy 1978, 1982; Morgan 1987; Morgan and Christy 1994, 1995; Kellmeyer and Salmon 2001). Exact causes of synchronized courtship, however, still remain largely unknown. No studies have found clear evidence that female receptivity synchronizes courtship.
Uca lactea has a particularly strong semilunar rhythm of activity (see Yamaguchi 1971; Crane 1975). For those populations studied to date (Murai et al. 1987; Severinghaus and Lin 1990; Yamaguchi 2001a, 2001b, 2001c; Kim and Choe 2003), the mating behavior of U. lactea is synchronous and peaks near to spring tide, a pattern which is consistent with other species of the genus. However, courtship cycles may vary depending on the environmental conditions. We were particularly interested in a population on Kanghwa Island, Korea, because the variation in the tides is greater (tidal amplitude ranges from 4 to 10 m) than other sites where populations of Uca have been studied (which are, in general, 50–200 cm). We predicted that a large tidal variation would affect the courtship rhythm of the species because it may affect foraging opportunities. We found that the courtship rhythm of the population in Kanghwa Island was different from other populations of U. lactea. We discuss the environmental and behavioral factors that could lead to changes in courtship rhythm within the species.
Materials and methods
Fieldwork was conducted at the intertidal mudflat in Kanghwa Island off the west coast of South Korea (37°35′N, 126°32′E) during the breeding season from 2 July to 2 August 2000. Mean air temperature during the observation period was 31.4°C (range: 28–38°C), and the mean surface temperature was 31.6°C (range: 27–37°C). Mean relative humidity was 67% (range: 49–82%). Monsoon rains fell on approximately 1 out of every 4 days (data obtained from the Kanghwa meteorological observatory).
The semi-terrestrial fiddler crab U. lactea (family Ocypodidae), which lives on the upper intertidal mudflat, is easily recognized by the male's exaggerated white claw on one side (Yamaguchi 1971; Crane 1975). It has been reported to live in the tropical and subtropical Indo-Pacific region, including Taiwan and Hong Kong, extending as far north as Japan and South Korea (Yamaguchi 1971; Kim 1973; Crane 1975). Each crab digs and holds a burrow (approx. depth: 40–50 cm), which is used as a shelter or breeding location (Crane 1975). When tides cover the crab's habitat, it retreats into the burrow and plugs the entrance with mud. In the breeding season from June to August (Yamaguchi 1971; Kim 2002), males dig their burrows deeper and may build a semidome structure (called 'hood' by Crane 1975) at the entrance. They then wave their major claws toward wandering females (see Murai et al. 1987 for details). The females choose the mating partner by sequentially entering ('visiting') the burrows of several males (Yamaguchi 1971; Kim 2002). The crabs copulate in the male's burrow or on the surface near the female's burrow (Yamaguchi 1971, 2000b; Murai et al. 1987; Severinghaus and Lin 1990).
Observations of behavior
Prior to the observation period, we selected a focal area where U. lactea male burrows were at relatively high density. We defined a 2 mx2 m plot with four 50-cm long PVC stakes connected by fine nylon straps. Crabs' burrows within the plot were numbered with flags made with colored tape on sticks.
The crabs emerge from their burrows and are active on the surface for about 8 h each day during the diurnal low tide. Hence, we recorded hourly behavioral patterns of the crabs for approximately 8 h after the tide receded from 2 July to 2 August. They were not active on the surface at night, in heavy rain, nor on extremely dried sediment when the temperature was very high (Yamaguchi 1971; Crane 1975).
Behavior pattern of the male Uca lactea
Male stands on the surface motionless for more than several min.
Male enters its burrow and returns to the surface carrying mudball and deposits it.
Male drags material from sediment with ambulatory legs and stacks it at his burrow to make a semidome.
Male takes bits of sediment with its small chela, gets them into the mouth filtering organic materials and leaves small pellets on the surface.
Male rhythmically extends laterally and folds its major claw toward females.
Male directs a major claw toward other crab without physical contact.
Two males try to push each other backwards or fight with major claws interlocked.
Each day, males active on the surface were categorized into three groups based on courtship behaviors. Males that displayed claw waving at least twice during the eight daily observation periods were called 'wavers' and the others 'non-wavers.' Wavers were divided into two additional groups: those that had semidomes were called 'semidome-holders' and those that lacked a semidome were 'non-holders.'
The relationship between male behaviors and female activity
Each day at low tide, we counted the frequency of active females on the surface in the focal area, most of which were burrow-holders and fed on sediment. As near to the same time as possible, we recorded the frequencies of waving males and feeding males on the surface. In order to determine whether male courtship activity or feeding activity was associated with the frequency of females, we regressed the frequency of waving males and the frequency of feeding males on the number of females.
Few active males were non-waving (non-courting) at neap tides. In sharp contrast, the number of non-waving males peaked near the spring tides (Fig. 2B). The number of waving males was lowest just prior to spring tides, began to increase at spring tide, and peaked 3–5 days after spring tide. Wavers were also predominant during the neap tide period. Among the wavers, 85% were semidome-holders and 15% were non-holders.
For the males, the majority of time on the surface was spent feeding (60.5%, n=759 out of 1,271 counts in total) or waving (29.1%, n=371). Very little time was spent dome building (1.3%, n=16 min), mudballing (3.3%, n=42), threatening (2.8%, n=36), combating (1.8%, n=23), or pausing (1.1%, n=14). The proportional frequency of seven types of behaviors differed significantly between flooded and non-flooded phases (X2=310.56, df=6, P<0.0001) (Fig. 3). Especially, the proportion of waving and feeding behavior was dramatically different between the two phases. During inundated periods, most of the active males fed on the mudflat. On non-flooded days, most males waved (Waving: X2=296.75, df=1, P<0.0001; feeding: X2=295.07, df=1, P<0.0001). Other behaviors showed no significant differences following sequential Bonferroni's correction (n=7 tests, including waving and feeding).
On Kanghwa Island, the pattern of synchronized courtship timing of Uca lactea was different from the courtship pattern of other fiddler crab species. Although male activity peaked at spring tides, courtship displays such as waving and semidome building peaked at 4–5 days after spring tides. In other species that show semilunar courtship rhythms, male courtship peaks around spring tides (Crane 1958; Zucker 1978; Greenspan 1982; Salmon 1987; but see Christy 1978). This general pattern has been interpreted as reproductive synchrony between males and females because females should copulate about two weeks before spring tides in order to incubate larvae and release them when the tidal stream is the fastest (Greenspan 1982; Salmon 1987).
Even for other populations of U. lactea courtship rhythm peaked near to spring tides. In a Japanese population, male courtship peaked at 2–3 days before spring tides (Yamaguchi 1971, 2000b). In Taiwan, while the number of active individuals on the surface did not show a great difference between the neap tides and spring tides, mating frequency peaked at spring tides, which suggests that male courtship also peaked at these periods (Severinghaus and Lin 1990).
One reason for the discrepancy of behavioral rhythms in the Kanghwa Island population of U. lactea may be due to the environmental differences between this habitat and that of the other populations and other species. For example, the only other fiddler crab species known to have interpopulational variation in courtship timing is U. pugilator (Christy 1978; Salmon and Hyatt 1983). In Florida, their courtship was reported to show peaks at neap tides, whereas other populations peak at spring tides (Christy 1978). The explanation for the difference was that stream velocity in Florida is higher in neap tides rather than in spring tides and females release larvae at neap tides to facilitate their escape from predators (Salmon and Hyatt 1983). At Kanghwa Island, however, stream velocity is higher at spring tides relative to neap tides. Maximum velocity is approx. 230 cm/s at spring tides and 50 cm/s at neap tides (data from National Oceanographic Research Institute of Korea).
The most probable cause of courtship near neap tides in the extreme tidal range at our study site appears to be the relationship between tidal flooding and food availability. Tides are the principal transport mechanism of food such as diatoms and other organic particles for the fiddler crabs. Furthermore, crabs feed on the water-containing sediment because wet conditions facilitate filtering organic materials from sediment (J. Christy, personsal communication; Reinsel and Rittschof 1995). In our study site, the habitat of U. lactea is not flooded for 6–7 days of the semilunar tidal cycle. In these periods, the drying of the habitat caused U. lactea to be food deprived.
Other populations of U. lactea probably suffer less from food deprivation. In Japan, the habitat of U. lactea in Amakusa-Masushima (Yamaguchi 1971) was flooded almost everyday by tides (M. Murai, personal communication). Information on the habitat in Taiwan was not available, but there is no evidence that the habitat of the crabs is subjected to drying up, because the crabs are generally active on the surface without interruption (Severinghaus and Lin 1990).
Food availability may thereby influence the timing of male courtship. Due to the limitation of food supply around neap tides in the habitat, fewer males were active on the surface and active males were not feeding. Feeding was most predominant in the few days before the spring tide. This is the period when other species are typically observed to be courting. U. lactea probably delays courtship toward neap tides in order to get sufficient energy during spring tides.
At the beginning of our study period in early July, many males waved their claws and relatively few fed, although a peak in the spring tide had just occurred. The behavior of the crabs appears to be contrary to our hypothesis that the crabs must feed when tides flood the habitat during spring tides and court when the habitat is dry during neap tides. Two hypotheses might explain this apparent contradiction. First, during the rainy season the study site is moistened by rains, enabling the males to feed even at neap tides and court at spring tides. However, although rainfall provides wet conditions for crabs to feed, it cannot provide crabs with fresh food because they only feed on organic matter that the tide deposits on the mudflat. Only flooding can provide food by a process of suspension and accumulation. Indeed, rainfall may delay courtship rhythm by interrupting males from feeding (T.W. Kim, personal observation). Second, a large tidal amplitude may accumulate more organic matter on the mudflat due to the higher floods. In early July, the spring tide was in the new moon phase, which is higher than the spring tide in the full moon phase (see Fig. 2A). Females as well as male crabs could begin to feed earlier in a new moon spring tide, encounter more organic particulate, and obtain sufficient energy to begin reproduction earlier. The data indicate that males can even court in the latter portion of the spring tide.
In a related study, we tested whether food availability influenced courtship timing directly by conducting food addition and removal experiments. We found that an increase in food availability advanced the timing of male courtship and increased the courtship intensity, whereas food deprivation had the opposite effects (Kim and Choe 2003). Hence, U. lactea males exhibit flexibility in the expression of mating behaviors in response to food availability.
Near neap tides when males were courting, female crabs sampled burrows occupied by males, and presumably assessed the male in each burrow. If a female stayed in the burrow for a long time (e.g., >15 min), the male came out of the burrow and the lone female plugged the burrow entrance presumably to oviposit. Then the male who lost his burrow wandered to find new burrows (T.W. Kim, personal observations). We are not sure if mating occurred in the male's burrow because females can use stored sperm obtained by surface mating to fertilize eggs (e.g., Koga et al. 2000). As a result of the females' lone activities in the burrows, however, during male courtship activities, a male biased sex ratio was evident on the surface. Waving males were most active when females were least active on the surface, whereas males were feeding when females were most active and also feeding.
In contrast, surface mating was more prevalent during spring tides. Males that mated on the surface neither built semidomes nor waved to females (n=16 out of 17 males). Most importantly, females mated with additional males after mating on the surface (T.W. Kim, personal observation). Hence during spring tides, many females may not be receptive and even those that mated may not have been fertile (Murai et al. 1987). As a result, males might not display courtship signals.
A corollary to the hypothesis that food availability influences male courtship activity is that it also influences female reproductive receptivity. Then perhaps it is the females' receptivity that triggers male courtship signals. As evidence to the contrary, the periodicity for female U. lactea reproduction in Japan was a lunar cycle, whereas that for the reproductive behavior of males was semilunar (Yamaguchi 2001a). Therefore, we propose that factors other than female receptivity and the female's response to food availability are influencing male reproductive behavior. Without experimental studies, it is difficult to determine which sex first attracts its mates. In this regard, we need to study how reproductive synchrony may be linked to various environmental factors such as food availability (Kim and Choe 2003), predation pressure (Christy 1978), male-male competition (Zucker 1984), and temperatures (Henmi 1989).
We are very thankful to John H. Christy at the Smithsonian Tropical Research Institute and Minoru Murai at the University of Ryukus and two anonymous referees for valuable comments. Delali Dovie improved this paper with valuable discussion and Michiko Sato provided help getting information in Japan. We also thank Sanha Kim, Youna Hwang, Ho Young Suk and other members of the Laboratory of Behavior and Ecology of Seoul National University for many helpful discussions on the results. We thank the National Oceanographic Research Institute of Korea for providing meteorological and tidal data cited in this study. The Korean Federation of Science and Technology Societies supported R.B.S. with a Brain Pool Professorship. This study was supported by the Brain Korea 21 Research Fellowship from the Ministry of Education and Human Resources Development.