Introduction

Monogamy has been reported in a variety of animal taxa, such as mammals, birds, reptiles, fishes and crustaceans (Kleiman 1977; Wittenberger and Tilson 1980; Wickler and Seibt 1981; Barlow 1984; Bull 2000; Reichard and Boesch 2003; Whiteman and Côté 2004). In some of these animals, the pair bond persists through several reproductive seasons (Black 1996). To understand the evolution of perennial monogamy, it is of great importance to clarify how and why the pair bond is maintained during the non-reproductive season.

Most of the studies carried out on pair association of monogamous birds in the non-reproductive season indicate that paired birds are in close proximity and exhibit behavioural synchrony in the same way as in the reproductive season (Hogstad 1992; Kellam 2003; but Gunnarsson et al. 2004). In monogamous fishes, perennially monogamous species are very few, and pair association in the non-reproductive season has been examined only in few species (e.g. butterflyfishes: Fricke 1986; Driscoll and Driscoll 1988; Yabuta 2007; the long-finned goby Valenciennea longipinnis: Takegaki 2001). As in monogamous birds, pair members of these fishes remain in close proximity all year around and coordinate their behaviour in foraging, nest construction, among others.

In the monogamous pipefish Corythoichthys haematopterus Bleeker, pairs mate in two successive reproductive seasons if both members survive (Matsumoto and Yanagisawa 2001). Mate changing occurs only after one of the pair members has died or disappeared (Matsumoto and Yanagisawa 2001). In the reproductive season, pair members of C. haematopterus engage in a ritualized interaction, called greetings, at a particular site early every morning (Sogabe and Yanagisawa 2007), like other monogamous syngnathids (C. intestinalis, Gronell 1984; Hippocampus fuscus, Vincent 1995; H. whitei, Vincent and Sadler 1995; H. zosterae, Masonjones and Lewis 1996; Hippitchthys penicillus, Watanabe et al. 1997). It has been suggested that daily greetings in monogamous syngnathids play an important role in the maintenance of the pair bond (Vincent 1995).

In the study reported here, we examined whether pair members of C. haematopterus exchange greetings daily during the non-reproductive season and whether the behavioural patterns of the greeting in the non-reproductive season are the same as those in the reproductive season. We also evaluated whether greeting pairs in the non-reproductive season are maintained until the pair breeds.

Materials and methods

This study was carried out using SCUBA equipment at Morode Beach (33°00′N, 132°30′E) on the west coast of Shikoku Island, Japan. Two quadrats (20 × 50 m and 20 × 25 m, respectively;depth 2–8 m) located approximately 50 m apart were each subdivided into grids of 5 × 5 m using a string. The bottom substrate (e.g. boulders, corals and artificial structures) within each quadrat was mapped on plastic paper (scale 1/100). Prior to the beginning of the study, all adult Corythoichthys haematopterus (>90 mm total length, TL; A. Sogabe personal observation) in the quadrats were collected using a hand net, measured for TL and then marked individually using a hypodermic injection of a VIFE (visible implant fluorescent elastomer; Northwest Marine Technology, Shaw Island, WA) to various sides of the body. Marked fish were caged for 1 day to recover from the handling stress and then released at the capture site. Throughout the study period, every unmarked adult C. haematopterus found in the quadrats was captured, measured and individually marked. This marking technique is commonly used in fishes and has been shown to have minimum impact on the animal (e.g. seahorse Hippocampus abdominalis, Woods and Martin-Smith 2004).

The quadrats were censused daily between 0930 to 1830 hours between 7 November and 14 December 2003 and between 2 March and 29 April 2004 (the reproductive season of this pipefish is early May to late September). The location of each marked fish was plotted on a map, and the location data were used to estimate its home range by measuring the area of the minimum convex polygon covering all daily census plots for each census period. If any behavioural interactions between conspecifics occurred, the identities, behavioural patterns (for details, see Matsumoto and Yanagisawa 2001) and positions of each individual fish were recorded.

To confirm the occurrence of greetings during the non-reproductive season, we randomly selected a focal male within the study site and monitored for greetings in a total of 34 males from 9 November to 9 December 2003 and from 3 March to 21 April 2004. Because greetings were exchanged within a few hours of sunrise in the reproductive season (Sogabe and Yanagisawa 2007), the observation of a focal male was carried out from just before sunrise to 0830 hours. If interactions with a female occurred, the type of displays observed was recorded together with the location, onset time and duration. The categorization of displays in the greeting followed that described in Matsumoto and Yanagisawa (2001). To determine whether a greeting pair during the non-reproductive season reflects the actual mating association in the following breeding season, we observed the mating behaviour of pairs in May 2004. We assessed a male and female to be a mating pair by the direct observation of copulation. Because of their low mobility and philopatry (Matsumoto and Yanagisawa 2001), individuals that disappeared from the quadrats and the surrounding areas were considered to have died.

Data from the two observation periods did not differ significantly (Mann–Whitney U test with Bonferroni correction; non-significant for all variables), allowing for data to be pooled for further statistical analysis. For data analysis, non-parametric statistics were used because most of the data distributions differed significantly from normality, even after appropriate data transformation. All tests were two-tailed and the level of significance was 5%. Data are given as the mean ± SD unless stated otherwise.

For the comparison of greeting behaviour between the reproductive and non-reproductive seasons, data from the reproductive season in 2002 were used (Sogabe and Yanagisawa 2007).

Results

In focal male observations, 32 of 34 males encountered a specific female and exchanged greetings only with her. For the other two males, which did not exchange greetings, one additional observation was made, but neither were observed to perform the greeting. The greeting of the 32 males all occurred in the early morning, mostly within 1 h of sunrise (Table 1), and the starting time positively correlated with sunrise (Spearman’s rank correlation r s = 0.859, n = 32, P < 0.0001). Males came to the greeting site earlier than their mates in 22 pairs, whereas females came earlier in seven pairs (the order of visitation was not observed in three pairs). This ratio significantly deviated from 1:1 (binomial test; z = 2.60, n = 29, P < 0.01). The greetings lasted about 3 min, involving a series of displays consisting of approach, cross, arch and both arch (Table 1). In 15 pairs, these greetings were repeated two to five times (2.9 ± 1.1 times) with a pause of a few minutes (6.6 ± 4.5 min). In these cases, many more displays were performed in total (33.7 ± 12.7) within 3–10 min (374.7 ± 139.4 s). Compared to the greeting in the reproductive season, the greeting in the non-reproductive season was characterized by a longer duration and higher repetition, resulting in a greater total number of displays (Table 1). However, there were no differences in the type and frequency of displays between seasons (Table 1).

Table 1 Characteristics of the greeting behaviour of pipefish Corythoichthys haematopterus in the non-reproductive and reproductive seasons (ns non-significant)
Full size table

The home ranges of a pair overlapped and also with that of other conspecifics (Table 2), but the size of the home range did not differ significantly between pair members (Wilcoxon’s signed rank test z = −0.524, n = 28, P = 0.60). In most cases, their greeting site was situated within the overlapped area of their home ranges (within the overlapped area, n = 15; within the male, not female, home range, n = 5; within the female, not male, home range, n = 3; outside the male and female home ranges, n = 5; chi-square test for goodness of fit χ2 = 12.57, df = 3, P < 0.01), and the distance between the greeting site and each home range centre did not differ significantly between pair members (Wilcoxon’s signed rank test z = −0.911, n = 28, P = 0.36; Table 2). After the time spent greeting, pair members rarely stayed in close proximity (percentage of time within 30 cm 13.7 ± 15.1%, n = 28), and even when they were observed to be close, no behavioural interactions occurred between them.

Table 2 Spatial relationship between home ranges and greeting site in each pair, and home range overlapping with other C. haematopterus conspecifics
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Of the 32 greeting pairs, 18 mated and 11 did not mate in the next reproductive season. The latter cases all occurred because both fish (n = 4) or the only female (n = 7) of the pairs had died during the non-reproductive season. All seven males whose mate had died were paired with a new mate in the reproductive season. In the three other greeting pairs, both members were alive in the next reproductive season, but we were not able to determine whether they mated within the season.

Discussion

Studies to date have reported the occurrence of greetings only in the reproductive season in a number of monogamous pipefishes and seahorses (Gronell 1984; Vincent 1995; Vincent and Sadler 1995; Masonjones and Lewis 1996; Watanabe et al. 1997). To the best of our knowledge, the present study is the first to quantitatively report the occurrence of greetings in the non-reproductive season among monogamous syngnathids.

During the non-reproductive season, soon after sunrise, we observed pairs exchanging a series of displays lasting a few minutes. This pattern of morning interactions between the sexes is basically the same as the greeting in the reproductive season (Sogabe and Yanagisawa 2007). No detectable differences were found in the type of displays between seasons, although there was a difference in the number of greetings: the greeting was repeated a few times with a pause in some pairs in the non-reproductive season, whereas the greeting was not repeated in the reproductive season, except for the day of spawning (Sogabe and Yanagisawa 2007). Since nearly all focal males chosen randomly (32 of 34 males) exchanged greetings only with their partner, it can be concluded that this behaviour occurs daily in the non-reproductive season as it does in the reproductive season.

The daily greeting of monogamous syngnathids in the reproductive season is believed to have two functions: the reproductive synchronization of a pair and the formation and maintenance of the pair bond (Gronell 1984; Vincent 1995). Our results show that the greeting pairs never broke up in the non-reproductive season and mated in the next season if both members were alive. This behaviour suggests that the daily greeting plays an important role all year around in the maintenance of the pair bond.

It is of interest that the daily greeting of C. haematopterus lasts only a few minutes and that the pair has few interactions, if any, during the daytime. The temporary interactions between pair members in C. haematopterus contrast with the behaviour of pairs in other perennial monogamous fishes, which stay in close proximity through the daytime to increase foraging efficiencies (butterflyfishes: Fricke 1986; Driscoll and Driscoll 1988) or to construct and maintain their burrow (the long-finned goby Valenciennea longipinnis: Takegaki 2001). One probable factor that accounts for differences in pair proximity between C. haematopterus and other perennial monogamous fishes is the necessity of cooperative activities in the latter.

Several hypotheses have been proposed to account for the evolution of the pair bond in the non-reproductive season. By maintaining the pair bond, pairs may derive direct benefits such as enhancement of the vigilance for predators (Hogstad 1995) or foraging efficiency (Scott 1980; Hogstad 1992) and/or indirect benefits in the following reproductive season by permitting the earlier onset of reproduction (Hall 1999), sequestering a known high-quality mate (Black 1996). among others. Ultimate factors for the evolution of off-season pair bonding in C. haematopterus must be related to indirect benefits because they do not cooperate in their activities. In the reproductive season, mate change is disadvantageous to either sex because of the time costs associated with it (Sogabe et al. 2007). It is therefore likely that the primary concern of both sexes is to secure a mate which accords with their reproductive potential rather than to seek for a mate of higher quality. The demand for stable pair bond will be strengthened if familiar partners improve reproductive efficiency.