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Simplicity and diversity in the reproductive ecology of triggerfish (Balistidae) and filefish (Monacanthidae)

HIROSHIKAWASE CoastalBranch ofNatural HistoryMuseum and Institute,Chiba, Katsuuna,Chiba 299-5242Japan

SUMMARY Reproductive ecology of 14 balistoid species (Balistidae and Monacanthidae) was reviewed. There are many common features in the reproductive ecology of the balistid fish: males establish territories; males and females mate in pairs on the sandy bottom; the pairs release gametes in a few seconds; eggs are small in size and a clutch contains large number of eggs; spawning occurs in the morning and embryos hatch after sunset of the day; females tend and guard the eggs at least Primitive monacanthid species show the same features of the balistids, however, reproductive ecology of the monacanthids is diverse. The evolution of reproductive ecology of the balistoidswas discussed referring to the phylogenelic relationships.

KEYWORDS: spawning behavior, parental egg-care mating system, territoriality, evolution

INTRODUCTION

Knowledge of reproductive behavior of reef fish has been REVIEWED SPECIES accumulated in the past thirty yews." Many of the studies were focused on the reproductive strategy of fish such as I review reproductive ecology of 8 species in 5 genera in parental egg care, mating system, mate choice and sex Balistidae, Odonus niger,10 Pseudobrahstes flavimargina change. For example, sex change has bean well studied in tus,13P. fuscus,10Xanthichthys mento,14Sufflamen chryso the labrid and gobiid fishes. Wamer4 theoretically explained the phenomenon with size-advantage model. pterus,15, 16 S. fraenatus,12 S veins,1 Rhinecanthus Kuwamura and Nakashima5 reported the other two factors, aculeatus,18and 6 species in 6 genera in Monacanthidae, growth-rate advantage and mortality-advantage, to expand Stephanolepis cirrhfer,19 Paramonacanthus japonicus,20 the model. Cantherhines pardalis,21 Rudarius ercodes22-24Oxymona On the other hand, few comparative, evolutionary studies canthus longirastris,11,21-27 Brachaluteres ulvarum.21 Most of reproductive behavior of fish have been done . The use of the studies are based on underwater observations of behavioral patterns in resolving phylogenetic relationships between species is increasing in importance, although results of aquarium observations are included. as the phyloganetic methods enable to trace the evolution Citation of literaturewas omitted as a rule in the following of behaviors in related taxa6, 7 However, data for descriptionswhen features of ecology common among the phylogenetic analysis are not enough in most groups at 14 specieswere described. present Balistdaeand Monacanthidaeare closely relatedfamilies SIMPLICITY IN BALISTIDAE included in the superfamily Balistoidea in Tetraodontiformes.8Approximately 40 species are known Spawning and eggs in Balistidae in 12 generain Balistidae and 100 species are known in 21 generain Monacanthidae.9 Fricke10reported parental care and mating system of the two balistid species, Spawning behavior of the balistid fish is simple (Table 1). Pseudobalistesfuscus and Odouns niger Spawning always occurs in a pair of male and female. No , based on field sneaking or group spawning has been reported. The pair observations. Barlow11reported a monogamous filefish, touches abdomens and release gametes in a few seconds. Oxymonacanthuslongirostris. In the past ten years, studies on both families increased and knowledge on Spawning site is usually sandy bottom or sandy reef reproductiveecology has accumulated Time of spawning is restricted to early in the morning .12 although that off memo is not fixed 14 In this paper, I review the reproductive ecology of the The balistid females release 55,500-430,000 eggs in a balistid and monacanthid fish . Spawning behavior, spawning. Eggs are spherical in shape measuring 0.47 Parental egg care and mating system are compared among 0.55 nun in diameter. They are demersal and adhesive, and between the two families . Furthermore, I discuss the evolution of reproductive ecology ofthe balistoid fish released eggs being attached to sand particles. Eggs of O. niger and X mento are scattered on the bottom and mixed 120

Table 1 Comparison of the spawning ecology and eggs in the balistid and not guard the eggs, resulting in maternal egg-cane. monacanthidfish Territoriality and mating system in Balistidae

It is common in the balistid males to establish a territory (Fig. 1). P. flavimarginatus and X memo males temporarily establish a territory for spawning and parental egg-care, but not for feeding 13,14 The other balistidmales establish a permanent territory for both spawning and feeding R aculeatus male remained in the same tenitory for 8 years.18 On the other hand, not all femalesestablish a territory * 1 Brachaluteres ulvarum females release eggs in2O-30 seconds. *2 Spawn (Fig. 1). P. flavimarginatusand X memofemales visit ingtime ofXonthichthys merto is not frxed *3 Eggs ofX. mento hatch on the male's territoryto mate13,14,O. niger femalesreside in next day of spawning. male'sterritory without establishing territories l0 Theother with sand", 14while those of the others are deposited in a balistidfemales reside in male'sterritory and eachof the mass. Eggs are cared for by parent(s) and the eggs hatch femalesestablishes smaller exclusive territories to theother in the evening on the day although that of X memo hatch residentfemales on the next day of spawning.14 Mating system is male-territory-Visiting (MTV) polygamy29in P. flavimarginatus and X mento,l3,14non tenitorial-female (NTF) polygyny12 in O. niger10and Parental egg-carte in Balistidae territorialfemale (TF) polygyny12in the other balistids(Fig Maternal and biparental egg-care is reported in the balistid 1). However, tenitoriality and mating system may change with some ecological factors and regions as reportedin P fish (Fig. 1). Parental egg-care consistsof egg tending and .fuscus. 10,13 egg-guarding.22 It is common in all the 8 species that females tend eggs by fanning and blowing water on them and guard the eggs by driving away intruding fish, and that DIVERCITY IN MONACANTHIDAE males never tend the eggs. The differenceof parentalegg care comes from whether males guard the eggs. Male O. Spawning and eggs in Monacanthidae niger, P. flavimarginatus and X memo guard the eggs, resulting in biparental egg-care.10,13,14The other males do Spawning behavior is diverse in the monacanthid fish

Fig. 1 Comparison of territoriality, mating system and parental egg-care in the balistid fish. 121

(fable 1). Spawning occurs in a heterosexual pair though and Balistoidea (Balistidae and Monacanthidae).31,32 groupspawning with one female and multiple males is also Phylogenetic analysis of the Balistoidea based on observed. Gametes are released in a few seconds anatomical characters clearly revealed that the characters althoughit takes 20-30 seconds in female B. ulvarum.28 are various in the Monacanthidae while they are very Spawningsubstratum is sandy bottom in S. cinrrgiferand P. simple in the Balistidae. Furthermore, the monacanthids japonicus,19,20algae in C. pardalis, R ercodes and O. longirosare more specialized than the balistids and the tris,11,21-25and calcareous sponges in B. ulvarum.28 monacanthids were derived from the balistids or, at least a Tim of spawningis restrictedin the morning in S cirrhifer balistid-like ancestor.' Here, I refer to the phylogenetic and R ercodes19,22,23while this changes according to the relationship and discuss the behavioral evolution of the watertemperatures in O. longirostris.27 balistoidfish. The monacanthidfemales release 160-17,500 eggs in a spawning. Eggs are demersal and adhesive, measuring Evolution of spawning 0.53-0.82mm in diameter. Eggs are deposited in a mass or scatteredon the substrata. Eggs of the balistid fish are depositedon the sandy bottom and attached to sand particles. This is also common to the Parental egg care in Monacanthidae phylogenetically primitive species of S cirrhifer and P. japonicas, while derived species utilize various objects as Papal egg-care is diverse in the monacanthid fish S spawning substrata (Table 1). It seems that the primitive cirrhiferfemale exhibits egg-care, however, it is restricted spawning substratum of the balistoid fish is sandy bottom. to a few minutes after spawning and no further parental Substratum requirments have broadened in derived cam is observed.19 Both male and female P. japonicus balistids while various additional substrata are used by showegg guardingand tending untilhatching for 2-3 days. monacanthids They care for multiple clutches on separate sites when Spawning patterns and features of eggs of balistids have spawningoccurs over successive days.' Maternal egg some common aspects with those of pelagic-egg spawning cam is common in R ercodes.20 Biparental egg-care is fish: gamates are released in a few seconds, eggs are small also observedwhen a parental male also guards the eggs in diameters; embryonic development goes fast and eggs aroundthe clutch Rarely, paternal egg-care is observed hatch within a day (Table 1). Furthermore, pelagic-egg when the male takes the female's position_22 No parental spawning species are reported in Triacanthidae which is egg-me is observedin the other three monacanthids. included in the most primitive group in Tetraodontiformes and Ostraciidaewhich is a family related to the Balistidae. Territoriality and mating system in Monacanthidae 33,34 The phylogenetic relationshipand spawning patterns suggest that the balistids may be derived from the ancestor Territorialityand mating systems of the monacarthids of pelagic-eggspawning fish. differamong species. An S cirrhifer male establishes a territory,in which 1-4 resident females establish smaller Evolution of parental egg-cane and mating system territories. Furthermore,non-resident females visit male's territoryfor spawning. Thus, the territorial male mates The different mating systems and patterns of parental rare with both types of females, mating system being TF among the balistids appear to be related to the distribution Polygynyand MTV polygamy m a single population.19 of food and breeding sites: those two are available in TF On the other hand, there is one resident female in P. polygyny mating system with maternal care although the japonicus and O. longirostris male territory; the mating former is limited or separated from the latter in the other system is monogamy.' R encodes males establish no two systems with biparental car.18 If egg tending territories. Dominant males pair with specificfemales , but (fanning) is essential for egg development and survival in matingdoes not always occur between the pair, the mating the balistids, evolutionary transitions have been from no systemis promiscuity22 care to maternal care instead of paternal care because one parent alone may not be able to allocate enough time to EVOLUTION OF REPRODUCTIVE BEHAVIOR fanning each of the multiple clutches.18 However, egg tending dose not seem to be essential for species such as X Phylogenetically, Tetraodontiformes is divided into three memo because most of the eggs hatch normally with much sub-order of Triacanthoidei, Tetraodontoidei and less frequent female tending," In this case, there is Balistoidei. Triacanthoidei is the most primitive, and another possibility in the evolution of parental care: Tetraodontoideiand Balistoidei have derived from the paternal care with egg-guardinghas evolved first and then common ancestor of Triacanthoidei. Balistoidei consists biparental care with additional egg-guarding and tending by of super-familyOstracioidea (Aracanidae and Ostraciidae) females has evolved. 122

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