Repetitive sex change in the stony coral Herpolitha limax across a wide geographic range

Abstract

Sex change has been widely studied in animals and plants. However, the conditions favoring sex change, its mode and timing remain poorly known. Here, for the first time in stony corals, we report on a protandrous (youngest individuals are males) repetitive sex change exhibited by the fungiid coral Herpolitha limax across large spatial scales (the coral reefs of Japan, Jordan and Israel) and temporal scales (2004-2017). In contrast to most corals, this species is a daytime spawner (08:00-10:00 AM) that spawned at the same time/same date across all the study sites. The sporadically scattered populations of H. limax among the coral reefs of Eilat (Israel) and Aqaba (Jordan) exhibited significantly slower growth, earlier sex change, and lower percentages of reproduction and sex change in comparison to the densely aggregated populations in Okinawa (Japan). At all sites, sex ratio varied among years, but was almost always biased towards maleness. Growth rate decreased with size. We conclude that comparable to dioecious plants that display labile sexuality in response to energetic and/or environmental constraints, the repetitive sex change displayed by H. limax increases its overall fitness reinforcing the important role of reproductive plasticity in the Phylum Cnidaria in determining their evolutionary success.

Figure 1

Herpolitha limax: a sequential hermaphrodite daytime spawner. (a) An example of a tagged individual (using a numeric plastic tag attached by a nylon fishing cord inserted through a thin hole drilled at the edge of the coral skeleton) monitored throughout the span of the study. A total of 480 individuals were monitored at the three study sites (175, 93 and 212 specimens in Okinawa, Eilat and Aqaba, respectively). (b) Male shedding spurts of sperm through multiple mouth openings. (c) Female shedding eggs through multiple mouth openings. In contrast to most corals, this species is a daytime spawner (releasing gametes between 8 am to 10 am for 5–7 consecutive days, five days after the full moon, of June-August or July-September). In all three study sites H. limax released gametes during the same months, same lunar age and at exactly the same time, in consecutive years.

Figure 2

Herpolitha limax (Okinawa, Japan): a heat-map displaying ‘expressed sexuality’ per individual coral (i.e corals whose reproduction had been studied for two years or more) throughout the study years. The cluster-aggregated boxplots to the right of the heat-map display the individual coral weight (g). Centerlines show the medians; box limits indicate the 25^th and 75^th percentiles; whiskers extend to min and max values and the range is colored in accordance with the legend below the heat-map; data points are represented by blank circles. n (from top to bottom) = 10, 21, 43, 22 individual coral weights. The color of each cell in the heat-map corresponds to the legend below it. Gray cells (ND) correspond to missing data and blue cells (NR) to non-reproductive coral. The rows (individual corals) are ordered by patterns of sexuality. Boxplot (a) – represents individuals that were documented only as ‘males’ throughout the study; Boxplot (b) – represents individuals that changed sex at least once but were not documented as having both gametes simultaneously (i.e. transitional); Boxplot (c) – represents individuals that were documented as containing both gametes simultaneously (i.e. transitional) at least once during the study. Boxplot (d) - represents individuals that were documented only as ‘females’ throughout the study.

Figure 3

Herpolitha limax: Size-frequency distribution of individuals for which sex was determined. Since individual corals in the population changed sex frequently, the calculation of size-frequency distribution was performed as an accumulation of data from all years. Data represent results from 2012 onward: Okinawa, Japan (2014–2017), Aqaba, Jordan (2013, 2015) and Eilat, Israel (2012–2017). Number of individuals (n) within each size group is indicated under the bars. Size groups (>1200 gr.) in Eilat contained only one individual indicated by (*) and are not shown in the figure.

Figure 4

Allometric relationship and size range at sex change of the monitored H. limax populations at Okinawa, Japan (2004–2017); Aqaba Jordan (2013–2016); and Eilat, Israel (2009–2017). Green triangles, males (M); red squares, females (F); gray X, non-reproductive (NR); orange circles, transitional stage (T). Number of individuals n (Okinawa) = 180, including 93 M, 57 F, 21NR and 9 T; N (Aqaba) = 178, including 39 M, 31 F, 103NR and 5 T; N (Eilat) = 157, including 45 M, 15 F and 97NR.

Figure 5

Herpolitha limax: average annual percentage increase in growth rate (weight) in different size groups, as measured at Okinawa, Japan (2004–2017); Aqaba, Jordan (2013–2016); and Eilat, Israel (2009–2017). Boxplot centerlines show the medians; box limits indicate the 25^th and 75^th percentiles; whiskers extend 1.5 times the interquartile range from the 25^th and 75^th percentiles; data points are represented by blank gray circles. Number of individuals (n) within each size group is indicated under the box.