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Intraspecific Egg Predation by Male Razorfishes (Labridae) During Broadcast Spawning: Filial Cannibalism Or Intra-Pair Parasitism?

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Intraspecific Egg Predation by Male Razorfishes (Labridae) During Broadcast Spawning: Filial Cannibalism Or Intra-Pair Parasitism? BULLETIN OF MARINE SCIENCE, 55(1): 133-141, 1994 CORAL REEF PAPER INTRASPECIFIC EGG PREDATION BY MALE RAZORFISHES (LABRIDAE) DURING BROADCAST SPAWNING: FILIAL CANNIBALISM OR INTRA-PAIR PARASITISM? Simon C. Nemtzov and Eugenie Clark ABSTRACT During field studies, we observed approximately 550 broadcast spawns (sometimes called pelagic spawns), in which pairs release their gametes high in the water column for external fertilization, by three congeneric wrasses: green (Xyrichtys splendens), rosy (X martinicensis) and pearly (X novacula) razorfishes. The released eggs formed a cloud that remained visible for 3-5 s before dissipating. Male X. splendens and X. martinicensis ate ova from the cloud during approximately 40% of their spawns. Male X novacula, and females of all three spe- cies, never ate ova. Our observations show that in fishes, parental care is not a prerequisite for filial cannibalism (the ingestion of one's own offspring), as was previously believed. Analysis of videotaped spawns showed that males were prepared to eat even before comple- tion of the spawning act. We propose that males may control the amount of sperm they release when engaging in spawning rushes. The eating behavior should be adaptive for ter- ritorial male fishes, particularly those with multiple daily spawns (we observed up to 23 spawns per day), because parasitism of nutrients from females (via the ova) may increase the males' chances for future reproduction, consistent with intraspecific predation theory. Filial cannibalism (the ingestion by an animal of its own offspring) seems to conflict with conventional evolutionary theory in that it apparently reduces the parent's fitness. Rohwer (1978) explained that filial cannibalism could be adaptive if a parent achieved higher future reproductive success by lowering its immediate fitness. He presented his model in terms of fish species with brood cycles, in which males defend temporary breeding territories where they guard eggs, and then, after the eggs have hatched, they abandon the territories to feed. He reasoned that by sacrificing part of the current clutch, a starving male might improve his chances of bringing the remainder of the clutch (and future clutches) to maturity. Hoelzer (1988) showed that intraspecific oophagy can occur in fishes with parental care but without brood cycling, and that filial cannibalism is, therefore, probably more common than was previously thought. Rohwer's (1978) model was written concerning partial-clutch cannibalism in fishes, but it may also explain whole-clutch cannibalism which necessarily ends any parental care of that clutch (Hoelzer, 1992). Partial-clutch cannibalism can also occur as a form of custodial care by parents when removing diseased or moribund eggs from the nest (Perrone and Zaret, 1979; Clutton-Brock, 1991). Although Rohwer's (1978) model does not differentiate between the eating of viable versus non-viable eggs, it is likely that both behaviors can be maintained by similar selective forces. Parents manipulate their investment in offspring to maximize their own fitness (Alexander, 1974). In filial cannibalism, the male effectively parasitizes nutrients from the female that he can then invest in future reproduction (Rohwer, 1978). For such intra-pair parasitism to be adaptive for the male, there must be a rea- sonable certainty that there will be future opportunities for him to reproduce. For tropical fishes that spawn daily all year-round, there is a high probability of future reproduction because the next spawning period is less than 24 h away. Intraspecific oophagy is common in many species of fish (FitzGerald, 1991; Katano, 1992). Filial cannibalism is a subtype of intraspecific oophagy in which 133 134 BULLETIN OF MARINE SCIENCE, VOL. 55, NO. I, 1994 the ingested eggs represent potential offspring. Filial cannibalism and nutrient parasitism would seem to be unlikely in broadcast spawning fishes (in which individuals release their gametes high in the water column), because eggs are fertilized and disperse almost immediately (Petersen, 199]; Petersen et aI., 1992). Yet, before they disperse, the eggs and sperm often form a temporary cloud which is sometimes exploited for food by planktivorous fish (Clark et aI., 1988; Colin and Clavijo, 1988). The appearance of this concentration of eggs can provide a brief opportunity for adaptive intraspecific oophagy. Recently there has been a great deal of interest in the prevalence of filial can- nibalism in teleost fish (Dominey and Blumer, 1984; FitzGerald, 1992; FitzGerald and Whoriskey, 1992), and its importance as a selective force in a wide range of behaviors and reproductive patterns (Foster et aI., 1988; Petersen, ]990). In pre- vious discussions, parental care was assumed to be necessary for filial cannibalism in fishes, as it allowed parents easy access to offspring. Yet in other vertebrates, filial cannibalism is relatively common under a wide variety of conditions, in- cluding cases with and without parental care (Polis, 1981), To fully understand the importance of filial cannibalism as a selective force, we must also consider fish species without parental care. Here we present observations of cannibalism of eggs during broadcast spawn- ing by males of two congeners with no parental care. STUDY SPECIES Green razorfish (Xyrichtys splendens), rosy razorfish (X. martinicensis) and pearly razorfish (X. novacula) are tropical wrasses (family Labridae) of the western Atlantic (Randall, 1965). They live on shallow grass or sand flats adjacent to coral reefs, where they forage on benthos and plankton. X. sp/endens and X. martinicensis generally live in single-male harems (Victor, 1987; Nemtzov, 1992). The mating system of X. novacula has not been described but it is apparently haremic (pers, obs.). All three species are protogynous hermaphrodites, i.e., they undergo sex change from female to male (Roede, 1972; Victor, 1987; Nemtzov, 1992). Like all tropical wrasses, razorfishes engage in external fertilization by broadcast spawning in which gametes are released when the fish are high in the water column. Razorfishes spawn only in pairs (Nemtzov, 1982, 1985, 1992; Clark, 1983; Thresher, 1984; Victor, 1987; Scarr, 1990), daily, during a late afternoon spawning period, all year-round (Clark, Shen and Scarr, pers. obs.). METHODS All three species of razorfishes were observed by stationary SCUBA divers in shallow (5-10 m deep) habitats around the southern Caribbean island of Bonaire, Netherlands Antilles (I2°N, 68°W) during February and June 1986 (by E.C.), and from June to August in 1989 and 1990 (by S.C,N.). Male X. sp/endens and X. martinicensis were identified by tags or natural markings, and were observed over the entire daily spawning period which began about 3 h before sunset and lasted 1.5-2 h. While watching focal males we noted the time each spawning occurred and whether or not the male ate eggs. Although we had observed many individual occurrences of egg eating, we present here data from 31 complete spawning periods of 15 male X. splendens, and II spawning periods of 7 male X. martinicensis (Table I). We also present data from 39 complete spawning periods of 6 male X. no- vacu/a (Table I) that were observed by Clark, Shen and Scarr (unpub!. data). Data from males with more than one spawning period are presented as individual means. An underwater videographic record (using ambient light) was made during some of the spawning periods of the razorfishes. Videotapes of 20 complete spawning rushes of the razorfishes were analyzed visually both in slow-motion and frame-by-frame. Sketches of behaviors (Fig. I) were traced from the screen of a television monitor in freeze-frame, and from single-frame print-outs. Figures ]a, and 1b were each drawn from a videotape of a single spawning rush, each with an elapsed time of about 5 s. The seven sketches in each of the two parts of Figure 1 were chosen as arbitrary representative views; they do not denote equal amounts of time between sketches, NEMTZOV AND CLARK: OOPHAGY BY RAZORFISH 135 Table 1. Intraspecific oophagy during broadcast spawning by Caribbean razorfishes (genus Xyrichtys) X. .\'{Jlendens x. martinicen.si.s X. novacula Total number of spawns observed 295 55 126 Spawns with egg eating, N (%)* 107 (36.2) 23 (41.8) o Number of complete spawning periods observed 31 II 39 Spawning periods observed per malet 1.6 ± 0.4, 1-4 1.6 ± 0.7, 1-3 7.8 ± 1.7,3-14 Spawns observed per spawning period:!: 9.5 ± 1.0, 3-23 3.2 ± 0.3, 1-4 2.7 ± 0.6, 1-8 * There was no significant difference between X. splendens and X. martmicensis in the percentage of spawns with egg eating; G = 0.15, df = I. P > 0.3; 2 X 2 G-test for the significance of the difference between two percentages (Sokal and Rohlf. 1981). t Mean ± SE, range. 4:Menn of individual males' means ± SE, range. OBSERVATIONS All three species of razorfish engaged in broadcast spawning, in which pairs rose quickly in the water column with their bodies touching along most of their lengths. At the apex of the spawning rush the two fish separated quickly ("snapped" apart), about 2-4 m above the substratum producing a small (diameter ca. 15 cm) white cloud in the water that dissipated in 3-5 s (Fig. I). We could sometimes discern individual ova within the cloud. After snapping apart at the apex of the spawning rush, both the male and female usually darted back down to the substratum (Fig. 1b). Occasionally, however, immediately after spawning, male X. splendens and X. martinicensis turned and ate from the cloud before it dissipated (Table I) and only then returned to the substratum (Fig. la). X. novacu- la were never seen exhibiting such intraspecific oophagy. Also, we have never seen this behavior by a female of any species. Slow motion analysis of videotapes of spawning rushes showed that those that occurred when males ate eggs differed from usual spawning rushes (Fig.
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