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Ephemeral Sexual Dichromatism in Quinca mirifra (Teleostei, Apogonidae), a Black Apogonid with Solitary Behavior.

Abstract

During their courtship behavior males Quinca minfica Mees 1966 exhibit a rapid dramatic color change, from their normal deep-black coloration to a brilliant silvery/white displayed on most of their body including areas of the dorsal and pelvic fins. Such a well-defined and striking ephemeral sexual dichromatism has not been previously reported in Apogonidae. It is suggested that this trait developed in Q mirOca because of the reproductive advantage that it conferred to an apogonid possessing a marked solitary/cryptic behavior and an appropriate physiological mechanism suited for such rapid and dramatic color changes.

Zusammenfassung

Wahrend der Balzzeit vollzieht sich bei den Mannchen von Quinca mirifra Mees 1966, em n rascher, dramatischer Farbwechsel: von der normalen tiefschwarzen Farbe zu einem leuchtenden Silberweig auf dem grogten Teil des Korpers einschlieglich Riicken- und Bauchflossen. Bisher gab es keinen Bericht iiber einen derartigen gut beschreib-baren und auffalligen Farbuncerschied als Geschlechts-merkmal bei Apogoniden. Diskutiert wird, ob sich diese Eigenheit bei Q. mirOca mit seiner vereinzelten bis ver-borgenen Lebensweise wegen des Vorteils fur den Fortpflanzungserfolg entwickelt hat, einem Apogoniden mit einem fur solche raschen und dramatischen Farb-veranderungen geeigneten physiologischen Mechanismus.

Resume

Pendant leur comportement de parade, les males Quinca minfica Mees 1966 montrent un changement de couleur rapide et spectaculaire, allant de leur coloration normale tres noire a un blanc argente brillant etale sur la plus grande partie du corps comprenant des zones de la dorsale et de la pelvienne. Un tel dichromatisme sexuel ephemere, bien defini et spectaculaire n'a jamais ete mentionne pour les Apogonidae. On suggere que cette caracteristique s'est developpee chez Q. minfica a cause de l'avantage repro-ductif confere a un Apogonide en possession d'un comportement solitaire/cryptique marqu6 et d'un meanisme physiologique approprie pour provoquer des changements de couleur aussi rapides et voyants.

Sommario

Durante ii corteggiamento i maschi di Quinca mirifica Mees 1966 mostrano un rapido e drastico cambiamento di colore, passando dalla normale colorazione nero scuro ad un brillante argenteo / bianco visualizzato sulla maggior parte del corpo, comprese le zone della pinna dorsale e delle pinne pelviche. Tale ben definito e netto effimero dicromatismo sessuale non e stato mai descritto negli Apogonidae. Si suggerisce che questa caratteristica si sia sviluppata in Q. mirifica a causa del vantaggio riproductivo conferito ad un apogonide che possiede un comporta-mento solitario/criptico e un meccanismo fisiologico appropriato adatto per questi cambi di colore rapidi e drammatici.

INTRODUCTION

With 347 valid species (Eschmeyer & Fong 2013), Apogonidae (cardinalfishes) is the seventh most speciose family among Perciformes. It is composed of a diverse group of relatively small, mostly marine and often brightly colored fishes. They are found in tropical and subtropical latitudes of the Pacific, Indian, and at a lesser degree, Atlantic Oceans, with their greatest diversity occurring in the Indo-Australian Archipelago (Allen & Kuiter 1994). Most apogonids inhabit shallow tropical coral reefs. However, several species are found in soft-bottom communities and estuaries (Chrystal et al. 1985, Allen 1993, Randall et al. 1997). In addition, some species occur in deeper waters, one genus is confined to temperate waters and another genus is composed of strictly freshwater species (Fraser 1973, Allen 1987; van Zwieten 1995, Fraser & Randall 2003, Fraser & Allen 2011, Fraser 2013).

Apogonids occur in a variety of habitats, from mangroves to drop-off zones, sea grass beds, spur and groove sections, and in sandy and rubble patches, but typically, particular species or small group of species are restricted to narrow ecological zones (Vagelli 2011).

Apogonids show important variability in social behaviors and in the reproductive process, including degree of gregariousness, territoriality; length of pair bonding, courtship displays, post-mating levels of mate fidelity, and length of embryo incubation (Vagelli 2011). Typically, apogonids form small groups or pairs. Some species occur in large aggregations and a few are found as solitary individuals (Randall et al. 1997, per. obs.).

The family's common name is derived from the red coloration present in a number of species. However, yellow, white, and brown hues are common in the family, and many species possess striped or barred color patterns (Randall et al. 1997, Mabuchi et al. 2006).

The presence of sexual dichromatism in teleosts (usually displayed by males, but also by females of several groups) is typically associated with an increase in conspicuousness. It has been generally explained by the action of sexual (intra and inter) selection or by the interaction between both sexual and natural selection (Robertson 1981, De Martini 1985, Kodric-Brown 1990, Beeching et al. 1998, Mabuchi et al. 2006).

In labroids, Robertson & Hoffman (1977) suggested that epigamic selection plays a much more important role than intra-sexual selection in the development of sexual dichromatism (though not for species possessing strictly haremic mating systems), and reasoned that despite being more costly to maintain than permanent dichromatism, natural selection would favor the development of ephemeral dichromatism in environments where continuous display of conspicuous signals would increase the risk of predation. However, even in well-studied groups of coral reef fishes, the evolutionary basis of sexual dichromatism is generally unresolved (De Martini 1985), and it is not clear to what extent nuptial coloration is constrained by phylogeny (Kodric-Brown 1998).

Thresher (1984), in his review of the occurrence of sexual dichromatism in coral reef fishes, noted that although conspicuous permanent sexual dichromatism most often coincides with polygamous species, temporary dichromatism is not clearly related to a particular mating system but rather is an intraspecific communication channel to express readiness to mate. In addition, studies on several families of coral reef teleosts showed no clear relationship between different types of sexual dichromatism and mating systems (Kodric-Brown 1998). Thresher & Moyer (1983) suggested an inverse relationship between the extent of sexual dichromatism and the complexity of courtship in Pomacentrinae, where courtship is most complex in monochromatic species, least complex in permanent and temporal dichromatic ones, and intermediate in species with ephemeral dichromatism (only displayed during courtship). However, the authors also suggested that temporal dichromatism plays different roles in the reproduction of different species and may be subject to different selective forces, and that attempts to generalize a single selective process across the range of sexual dimor-phisms in any comparable group of fishes would likely prove unproductive.

Evident sexual dimorphism is largely absent in Apogonidae (Barnett & Bellwood 2005, Okuda et al. 2002, Randall & Fraser 1999, Vagelli 2011). Lachner (1953) reported that females of several species of Szphamia Weber, 1909 (a genus composed of species of a small size) average larger size, while males have a deeper body and a longer and deeper head, a dimorphism that he did not observe in the larger species of the family.

A few cases of putative permanent sexual dichromatism have been reported but consisting in rather minor variations in color or pattern. Lach-ner (1953) described adult males Fowleria isostigma (Jordan & Sale 1906) with duskier body coloration than females; Garnaud (1950) described males Apogon imberbis (Linnaeus 1758) as a bit smaller and with a deeper darker coloration; Gon & Randall (2003) observed males Ostorhinchus cookii (Macleay 1881) having a wider stripe in the base of the second dorsal fin and Myers (1999) described mature males Cheilodipterus singapurensis Bleeker, 1859 possessing a dark spot around the anus.

Temporary sexual dichromatism seems not to be common either. At least it is not conspicuous enough to be easily observed (e.g., during his extensive field surveys and taxonomic work in Apogonidae, Allen did not observe apogonids displaying color changes [Allen, per. comm.]), or worth mentioning when referenced to the reproductive behavior of the family (e.g., Allen 1993, Randall et al. 1997).

Among the approximately 20 apogonids whose nuptial and mating behaviors have been observed, color change was not present in Ostorhinchus cyanosoma (Bleeker 1853) (Thresher 1984, per. obs.), 0. hoevenii (Bleeker 1854) (per. obs.), 0. jenkinsi (Evermann & Seale 1907) (per. obs), 0. notatus (Houttuyn, 1782) (Kuwamura 1983), Sphaeramia orbicularis (Cuvier 1828) (Allen 1975), Pterapogon kauclerni Koumans, 1933 (per. obs.), Vincentia conspersa (Klunzinger 1872) (per. obs.), Zoramia fragilis (Smith 1960) (per. obs.) or Z. lep-tacanthus (Bleeker 1856) (pers. obs.). Variation in color intensity (i.e., fading/lightening, increasing intensity of the normal coloration) associated with breeding behavior was reported in two Apogon spp. (Thresher 1984), Ostorhinchus doederleini (Jordan & Snyder 1901) (Kuwamura 1985) , Cheilodipterus quinquelineatus (Cuvier 1828) (Kuwamura 1987), and Apogon quadrifitsciatus (Cuvier, 1828) (now in Ostorhinchus) (Saravanan et al. 2013). In males Apogon imberbis, Garnaud (1950) described a lightening of the normal red color (however, no variation was noticed during breeding behavior observations conducted in the wild (Mazzoldi per. comm.). A minor color change was reported in two instances. Chave (1978) observed Pristiapogon tae-niopterus (Bennett 1836) developing black fin markings when courting, and Fishelson (1970) observed a male Cheilodipterus lineatus (Lacepede 1801) partially fading its normal longitudinal striped pattern and developing a white vertical band on his trunk during courtship.

As far as it is known, the only reported case of an apogonid displaying evident temporary color change during breeding behaviors is Apogonichthy-aides Inger (Doderlein 1883). In this species of dark brown-bronze to blackish coloration, Kuwamura (1985) observed females changing color to whitish, and males developing three or four dark vertical bands during courtship.

Quinca mirifica is a large apogonid that in captivity can reach a standard length over 120 mm. It is confined to the western coast of Australia (records of the Western Australian Museum (WAM) show Q. mirifica was collected from approximately 13[degrees]45' to 22[degrees]07' Latitude S). Its description was based on a single specimen collected in 1959 on a reef habitat of Cockatoo Island and deposited at the WAM.

During day hours this species remains well hidden in rock overhangs in shallow reef areas (per. obs.), and under captive conditions within provided artificial habitats. Except for its reproductive biology, which includes the absence of a larval period (Vagelli 2011), virtually nothing is known about the natural history of Q. mirifica. The author's observations both in the wild and laboratory indicate that this apogonid possesses unusual marked solitary/territorial behaviors.

This paper reports a remarkable ephemeral sexual dichromatism in males of Quinca mirifica. A combination of particular behavioral and physiological mechanisms can explain the presence of such striking color change in this species.

MATERIAL AND METHODS

Collection, holding system and general conditions.

Ten adult specimens were collected with nets in November 2005 off the Gulf Coast and Mangrove Bay (Exmouth, Western Australia) and shipped to the author's laboratory in New Jersey. Shortly after their arrival, the specimens showed extremely agonistic behavior towards each other and were isolated. They were maintained in three recirculating systems, each one with two 400 L fiberglass tanks (119 x 58 x 58 cm deep) with a glass front. Each tank was partitioned either into two or three equal sections using dividers, built with PVC frame and a plastic mesh. Rocks and 10 cm diameter PVC pipe sections were used to fabricate hiding places for each specimen. The bottoms of the tanks were covered with a 1 cm thick layer of gravel and crushed coral. Filtration for all systems included a biofilter, an ultraviolet filter and activated carbon. Each tank was illuminated by two 40 W fluorescent tubes, with a photoperiod of 12 hL:12 hD. Artificial sea water was utilized (salinity ranged between 34-35[per thousand]), and temperature was kept at 27 [+ or -] 0.5[degrees]C. Daily feeding (ad lib.) consisted of chopped mussels Perna canaliculus, krill Euphasia spp. and smelt Osmeru.s sp.

Behavioral observations.

Courtship displays were observed in nine of the 10 original wild-caught specimens (six males and four females, one female died a few days after arrival). In addition, courtship displays were observed in 10 females and eight males bred and raised to adult stage in captivity. These observations took place over a four year period during which a larger study on the reproductive biology, embryology and growth was completed.

Since Q. mirifica lacks apparent secondary sexual dimorphism, several pair combinations were tried by joining 2 individuals in a tank section. The pair selection was decided by observing the behavior of two specimens separated by a divider. If the individuals did not show agonistic displays and showed signs of apparent receptiveness (e.g., by both remaining close to the divider and following each other with slow movements for extended periods) and showed no aggressive behavior, such as sudden burst of movements facing each other and attempts of biting through the divider, they were considered a potential pair and the divider was removed. If no signs of aggressiveness were evident, they were maintained together. After mating, the pair was separated and the brooding male was isolated during the entire incubation period. The pair's behavior was observed daily for several hours, generally from 10:00 to 15:00 h., until mating occurred.

RESULTS

Reproduction in Quinca mirifica involved transient pair formation, and a series of courtship displays and mating behaviors similar to those described in other apogonids, including side-by-side swimming and trembling, nuzzling, warping, and mouth-opening by the male (Kuwamura 1983, 1985, Vagelli 1999). As in other apogonids, females behaved as the "aggressive partner" (Thresher 1984), while males remained mostly passive, following the female's courtship with a rather submissive behavior, even letting themselves to be gently pushed and cornered against substrates. In addition, females Q. mirifica showed a distinct "holding" mating behavior. It consisted of maintaining the male with an extended pectoral fin, while the male remained inactive in an almost horizontal position. After the pair positioned side by side and the fish joined the ventral edge of their body, they began separating dorsally until forming an angle of approximately ninety degrees. The female held the male with her pectoral fin totally expanded, while the ventral line of both individuals remained in contact. During "holding" behavior, males remained almost motionless resting on the female' s pelvic fin, and allowing passively to be moved up and down by the female. This behavior persisted for extended periods lasting up to 2 hours interrupted by brief pauses of a few seconds.

The breeding behavior of males included a very striking display involving a sudden change in coloration. The changes in color and color pattern consisted of a rapid (3-10 seconds) fade of the normal deep black coloration (Fig. 1A-B-C) into a brilliant silvery/white that affected most of the male's body (Fig. 1D). The change excluded the head region, from the snout to approximately the insertion point of the pectoral fins, and a narrow section in the caudal peduncle, from about the margin of the caudal fin and extending forward a distance of about six scales. The color pattern of dorsal, pelvic, and anal fins were also significantly affected. The most conspicuous change occurred in the second dorsal fin, where the proximal half became white and contained two large black spots (Fig. 1D). The pelvic fins developed four large white blotches extending from about the fin origin to about 3/4 of the fins' length. In the anal fin, an elongated white mark appeared across the middle of the fin. The caudal fin, which normally has white color, and the pectoral fins, which are transparent, remained unchanged (Fig. 1D-E-F).

Color change typically occurred within a minute after a female approached the male and displayed signs of spawning readiness (mating behaviors). Males displayed the brightest white silverfish courting color pattern for relatively short periods, usually no longer that -2 minutes. Then, in most observed events, it rapidly faded to the normal all black coloration within a few seconds, but in some instances the courting pattern did not fade away completely, and males presented an intermediate greyish opaque-white hue for another 1-2 minutes.

After the males' color change display, the pair engaged in mating behaviors, particularly "holding" behavior, and males did not repeat the courting color pattern again (if the pair did not interrupt and completed the mating-spawning process).

Ephemeral dichromatism was displayed by all 14 males included in this study. It occurred in 23 out of 26 observed mating events: 13 of the 15 mating events involving the six wild-caught males, and in 10 out of 11 mating events involving eight males of captive raised Fl. In addition, in two instances males were observed displaying similar color changes when they occupied the same tank (but separated by a divider) with a mating pair. In both instances the color change occurred when the pair in the adjacent partition was engaged in courting behaviors (including ephemeral dichromatism by the other male) and the mating pair was situated very close to the divider.

In three breeding events, involving two different males, color change were not displayed during the observation time, and it included one instance in which the female was less persistent than usual in her courtship displays (in three occasions she moved away from the male and stayed separated for about one minute). Despite the absence of male's color change, mating occurred in all three instances. Thus although ephemeral dichromatism was a typical component of the male's courtship display, mating in Q. mirifica might occur in the absence of male's color change (at least under captive conditions where the members of the pair were maintained very close).

In addition, similar striking color change was displayed by two males to each other (Fig. IF). The males were captive raised individuals of approximately two years of age and were the only occupants of a (divided) tank for four weeks. During this period, the males regularly showed marked agonistic bouts to each other, i.e., both individuals aggressively approached and faced each other, and tried to bite/engage each other through the divider. In addition, two- three times a day, generally in the morning-noon hours, they were observed displaying to each other. At the time of color change, males moved apart from the divider and behaved much less aggressively. 1 hey positioned on a narrow angle, sometimes parallel to each other, and they moved slowly within -20 cm from the divider. These male to male ephemeral displays were observed on an almost daily basis, and they lasted significantly longer (sometimes up to 10 minutes) than when displaying to females.

DISCUSSION

As opposed to labroids and pomacentrids, and to other typical coral reef fish families such as Scari-dae and Pomacanthidae, conspicuous permanent sexual dichromatism seems to be absent in Apogo-nidae, and as mentioned before, a few cases of minor temporary variation in color intensity have been reported. In addition, the scarcity of longterm field observations on individual mating pairs has led to a subjective and often inconsistent characterization of the apogonid mating patterns (Va-gelli 2011).

Kuwamura (1985) suggested a relationship between social behavior (gregarious vs. solitary) and reproductive behavior (length of pair formation) among several apogonids he studied. He described Apogon niger (now in Apogonichthyoides [Fraser 8c Allen 2010]) and Apogon doederleini (now in Ostorhinchus) as solitary species that formed transient pairs, with similar pre-spawning and courtship behaviors, whereas Apogon notatus (now in Ostorhinchus) as a gregarious species that formed lasting pairs and displayed distinct pre-spawning behaviors the day they mated (the prolonged- up to several weeks- pair bond occurred prior to spawning and females mated with different males, hence lasting pairs did not imply monogamy, [Kuwamura 1985] ). The gregarious species was monochromatic, 0. doederleini exhibited a minor color fading/intensification during mating (both sexes) and A. niger displayed a marked color change (both sexes, particularly females) (Table I).

Table I. Relationship between observed social and
reproductive behaviors, and presence of ephemeral
sexual dichromatism in Apogonidae.

Species              Color pattern      Social      Pair
                                       Behavior    Bonding

                                      Sol.  Greg,  Tran.  Last.  None

Apogon gonosome    Striped                  x      x             x
                   siiver-yellow/red

A. imbtrbis        Red                      x (1)  x             x
                                                                 (2)

Apogonichihyoidts  Dark               x            x
niger              brown-blackish     (1)

A. tatnktus        Striped            x            x             x
                   gray-yellow

Ostorhincbus       Yellow, black            x (1)  x             x
doedtrleini        striped                                       (2)

0. faciatus        Silverish-reddish        x      x             x
                   brown striped                                 (2)

0. hoevenii        Yellow-reddish           x      x             x

0. jtnkinsi        Red                      x      x             x

0. naiatus         Mostly                   x             x      x
                   yellow-reddish

Cheilodipterus     Brown-reddish            x      x             x
linmttts           white-striped                                 (3)

C quinquiUnratus   Striped                  x      x             x
                   black-yellow                                  (2)

fttrspogon         Verr. striped            x      x             x
kaudtmi            black-silverish

Sphaeramia         Dotted                   x      x             x
orbicularis        brownish-gray

Quince mirijica    Deep black         x            x

Vmcentm conspma    Dark red-brownish        x      x             x

Zortmia fagilis    Clear-yellowish          x      -      -      x

Z. lepmcantbus     Light yellow-with        x      x             x
                   blues

                    Ephemeral Sexual
                    Dichromatism

                   Evident  Dramatic    Author

Apogon gonosome                       Thresher
                                      1984, per,
                                      obs.

A. imbtrbis                           Mazzoldi
                                      et al.
                                      2008, per.
                                      com.

Apogonichihyoidts  x                  Kuwamura
niger                                 1985

A. tatnktus                           Kuwamura
                                      1985

Ostorhincbus                          Kuwamura
doedtrleini                           1985

0. faciatus                           Saravanan
                                      et al.
                                      2013

0. hoevenii                           Per. obs.

0. jtnkinsi                           Pers.
                                      obs.

0. naiatus                            Kuwamura
                                      1983

Cheilodipterus                        Fishelson
linmttts                              1970

C quinquiUnratus                      Kuwamura
                                      1987

fttrspogon                            Vagelli
kaudtmi                               1999

Sphaeramia                            Allen
orbicularis                           1975

Quince mirijica             x         This wotk

Vmcentm conspma                       Per. obs.

Zortmia fagilis                       Per. obs.

Z. lepmcantbus                        Pers.
                                      obs.

(1) Kuwamura (1985) referred to 0. doederleini, and A.
imberbis as solitary, however both species have been
found forming groups (e.g., Marnane & Bellwood 2002,
midietal. 2008). A. 'tiger was described possessing
solitary behavior, but individuals were found separated
by just "a few feet" Kuwamura (1985), and photographs
taken in the wild
(http://fishpix.kahaku.go.jplfishimage-e/search.html,
e. g., KPM-NR0040140, 0040887, 0035049)
would indicate that in some instances A. niger
forms small groups.

(2) It displays minor changes in its normal color
pattern such as fading, paling or increase in
intensity of colors

(3) It displays more marked changes in its normal
color pattern, such as fading longitudinal
stripes and developing vertical band.


In addition, eight species are known to be gregarious monochromatic that form transient pairs and have courtship displays lasting from a few hours (as in Vincentia conspersa) to up to 2-3 days (Ptera-pogon kauderni). Three gregarious apogonids (one Ostorhinchus and two Cheilodipterus spp.) possess a similar mating pattern (transient pairs) but differ in the degree of ephemeral dichromatism. Out of the other two apogonids reported as solitary (both form transient pairs) one, Apogonichthyoides taenia-tus (Cuvier 1828), is monochromatic whereas the other (Quinca minfica) presents a highly conspicuous temporary dichromatism (Table I).

Thus, there is no evident relationship between described mating patterns, social behaviors and the presence/degree of ephemeral sexual dichromatism in studied apogonids. This would agree with Thresher's (1984) characterization that ephemeral sexual color changes are not related to particular mating systems, but rather function as intraspecific signals to express readiness to mate.

Quinca mirifica is the first described apogonid displaying a very conspicuous ephemeral sexual dichromatism (males). Such a dramatic temporary color change is probably rare in Apogonidae, and it seems plausible that its development in Q. mirifica was product of two main factors, i. e., ethological (solitary behavior) and physiological (black coloration).

Quinca mirifica exhibits solitary behavior and crypticness, which is due to its black coloration and seeming tendency to remain hidden in dark reef overhangs or crevices. Under these circumstances, a male that effectively advertises his presence and indicates his readiness to mate to a wandering female, is likely to significantly increase his chances of reproducing, and the development of even a slight advertising color would have an immediate selective advantage (1). However, becoming conspicuously bright white-silverish in a dark environment would likely also increase predation pressure. Thus, in Q. mirifica ephemeral sexual dichromatism may have evolved subjected to both epigamic and natural selections, leading to the development of a brief nuptial display that does not even persist during the actual mating/eggtransfer (which is particularly prolonged in this species) reducing predation exposure (Fig. 1B-C).

-The finding of only isolated individuals in the wild (occurring tens or even hundreds of meters apart), and the territorial and conspecific agonistic behavior exhibited in captivity (remarkably, even by newly released recruits), suggests that Q. mirifica may be one of the less gregarious apogonids. However, if solitary behavior and formation of transient pairs would have been an important selective force in the development of a conspicuous sexual dichromatism in Q. mirifica, one may ask why other apogonids displaying a similar mating pattern and possessing relatively solitary behavior haven't been observed developing such a striking ephemeral color change?

A possible reason may be related to a second main factor, i.e., the physiological characteristics of the unusual black coloration of Q. mirifica, which is well suited for such a quick color change.

Color changes in teleosts are due to the aggregation/dispersion of pigment within the light-absorbing chromatophores, in particular to the motile activity of melanosomes, and to the reflecting changes in active iridophores (Beeching 1995, Fujii et al. 1989, Fujii 2000).

Fishes commonly present two main types of light scattering/reflecting chromatophores; i.e., leucophores and iridophores. Leucophores scatter light of wide wavelengths in all directions, they appear whitish when illuminated, and the light reflection is diffuse. Iridophores contain reflecting platelets, mostly composed of guanine crystals, and are responsible for reflection of light. In the case of non-motile iridophores the platelets behave as ideal multilayer reflectors and generate the silvery glitters and whiteness (Herring 1994, Fujii 2000, Mahtger et al. 2003).

In addition, different types of chromatophores can be positioned adjacent to each other forming "chromatophore units". Some are simple units made of melanophores and leucophores, or melanophores and iridophores, and the synergistic action of the chromatophores that form these simple units responding to neural changes is the basis of rapid color changes (Herring 1994, Fujii et al. 1989, Goda & Fujii 1998).

Most chromatophores are subjected in some degree to hormonal regulation. In melanophores, the melanophore-stimulating hormone induces the dispersal of melanosomes (darkening), whereas both the melanin concentrating hormone and melatonin (MT) have the opposite effect, resulting in a pale or bleaching color (in darkness, both sexes of Q. mirifica lose its deep black color, and a pale-brownish light grayish coloration generally covers the entire body, suggesting melanophores in this species respond to MT as described in other fishes, e.g., Aspengren et al. [2003]). However, it is the neural system that primarily controls the melanophores and is responsible for the rapid chromatic changes (Fujii 2000, Mahtger et al. 2003).

Melanophores display higher motile activity than other chromatophores such as xandiophores and erytrophores in response to neural stimulation, which results in melanophores having a leading role in quick color changes (Fujii 1993). In addition, the response to neural stimulation of melanophores and leucophores is opposite: whereas in melanophores the action of neurotransmitters induces the rapid aggregation of melanosomes (and hence fading of the black coloration), in leucophores it induces the dispersion of pigment (whitening), and because the melanophores and leucophores that form chromatophore units may be innervated by the same fibers, this opposite response occurs simultaneously.

Thus, the striking color change in Q. mirifica could be explained by the action of the synergic action between melanophores and light reflecting chromatophores as described in other teleosts (Fujii et al. 1989). In this case, the rapid fading of black color in extensive areas of the body would be due to the action of neurotransmitters released during "excitement" upon melanophores. The simultaneous appearance of the white and silver coloration could be the product of both the dispersion of leucosomes (product of the same nervous stimuli that caused the aggregation of melanosomes) and the exposure of non-motile iridophores to incident light.

In conclusion, the described combination of ethological-physiological characteristics in Quinca miri-fica is unusual in Apogonidae. Most apogonids exhibit some degree of gregarious behavior and mates are typically available. Moreover, apogonids present a large variety of color patterns (there are many species with little pigmentation) but they are generally based on combinations of reds, yellows, and to a lesser extent blues, and the chromatophores containing these pigments are not as well suited for rapid color changes as the melanophores are.

It is suggested that the striking sexual ephemeral dichromatism in Q. mirifica may have developed by conferring a reproductive advantage to males of an unusual species that possesses a marked solitary/cryptic behavior, and the seemingly appropriate physiological mechanism suited for such rapid and dramatic color change. Moreover, it is expected that such a conspicuous color change will only be found in apogonids presenting both solitary behavior and a dark brown/black (i.e., mostly melanophoric) coloration.

ACKNOWLEDGEMENTS

Thanks to Gerald R. Allen, Glen Moore, and Barry Hutchins for providing valuable advice and information that led to the successful collection of Q. mirifica. I am grateful to Jonathan Potter for his significant help in locating and capturing Q. mirifica. Thanks to Lyle Squire Jr. for his key collaboration in the shipping of live specimens to USA. Thanks to Thomas Fraser for updating the generic nomenclature.

Received: 13 June 2013--Accepted: 05 December 2013

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(1.) Despite the mentioned instances of intrasexual color change in captive males (Fig. 1F), it is unknown if such intrasexual displays occur under natural conditions. The observed adult solitary behavior in the wild is consistent with the observed unusual agonistic behavior displayed among new recruits in captivity Thus, the significance of male-male ephemeral dichromatism under such artificial conditions (where males were held in close proximity) and hence to what extent intra-sexual selection might have played a role in the development of sexual dichromatism in this species are uncertain.

Alejandro A. Vagelli

New Jersey Academy for Aquatic Sciences. 1 Riverside Drive, Camden, N.J. 08103. Email: avagelli@njaas.org
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Publication:aqua: International Journal of Ichthyology
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