Notes on the biology, geographic distribution, and conservation status of the Banggai cardinalfish Pterapogon kauderni Koumans 1933, with comments on captive breeding techniques.
The aim of this article is to bring to the hobbyist and aquarium community a summary of what is known to date about different aspects of the biology and conservation status of Pterapogon kauderni. In addition, I hope this review will help readers to appreciate its uniqueness among coral reef fishes, and will contribute to raising awareness with respect to the threatened status of its populations and habitat.
Introduction
The information presented here represents some of the results obtained during the last several years at the New Jersey State Aquarium (NJSA) in our research on the Banggai cardinalfish. The laboratory phase began in early 1997 and focuses on its reproductive biology, ecology, biogeography, evolution, and conservation, and included the development of a captive-breeding program. The fieldwork, which began in 2001 and continued in 2002, has been carried out in collaboration with Mark Erdmann (NRM/EPIQ, Sulawesi, Indonesia) and with financial support from the NJSA, The American Zoo and Aquarium Association (AZA), and The National Geographic Society.
For a detailed description on reproductive biology (including mating behavior, embryology, and juvenile development) see Vagelli (1999), for ecology and conservation see Allen (2000), Erdmann & Vagelli (2001), and Vagelli & Erdmann (2002).
BRIEF HISTORIC AND SYSTEMATIC REVIEW
The first time science learned of P. kauderni was in February 1920 when Walter Kaudern, during his 1917-1920 expedition to the Celebes Island (Sulawesi), collected two specimens close to the shore of Banggai Island and sent them to the Leiden Natural History Museum. Thirteen years later Frederick Koumans described the specimens as a new species and genus. He created the genus Pterapogon on the basis of the higher number of rays of the second dorsal fin, which distinguishes this genus from the rest of the apogonid genera.
In his 1972 work on Apogonidae, T. H. Fraser created the subgenus Pterapogon to differentiate the Banggai cardinalfish from Quinca mirifica, a cardinalfish from Northwestern Australia described by Mees in 1966, which Fraser classified within the genus Pterapogon (and subgenus Quinca). In November 1994 ichthyologist Gerald Allen and underwater photographer Roger Steen traveled to Banggai Island hoping to find this beautiful species, which fish guidebook author Kal Mullet had found in that area about two years earlier. In 1995 Allen and Steen published their observations on some ecological aspects of this species, and were the first to speculate about this species lacking a planktonic dispersal phase, and its connection with a very restricted geographical distribution. In 1997 the NJSA began a comprehensive research project on this species.
In 2000 a small population was detected in the Lembeh strait (North Sulawesi), the probable result of an accidental escape from holding nets that an exporter kept in that location.
Reproductive Biology
P. kauderni has a unique set of reproductive characteristics that makes it an exception among coral reef teleosts, e.g., it lacks a planktonic interval (its eggs do not enter into the plankton, and it lacks a larval period); therefore, this species does not have planktonic dispersal; it has very low fecundity; the male mouthbroods the egg-clutch for about 20 days, and after hatching, the embryos remain in the parent oral cavity for about 10 days until completion of development and release as juveniles. The brooding male does not eat during the entire incubating period, which lasts about 30 days.
PRESPAWNING BEHAVIOR
P. kauderni is a mouthbrooder in which transient pairs are formed and only the males incubate the eggs. Mating is preceded by an elaborate courtship that lasts normally several hours, but may extend to a few days. Prespawning behavior is composed of several courtship displays (female trembling, warping, side to side swimming, nuzzling and mouth-opening by the male).
The most characteristic prespawning display is the side-by-side trembling by the female (see Vagelli, 1999 for a detailed description of pre- and post-spawning behaviors). Side-by-side trembling normally lasts several hours. The only sign of a male's receptiveness is a conspicuous darkness along the lower jaw and sporadic mouth opening displays.
Spawning and Egg Transfer
P. kauderni reproduces all year long under laboratory conditions. Pair formation and courtship usually begin early in the morning and mating occurs during the first hours after noon. There is no secondary sexual dimorphism in this species. Therefore, the only method to differentiate sexes is to keep several individuals together and wait for the formation of pairs. Eventually, mature females will display an enlarged abdomen. Also, during pre-spawning behavior sexes are easy to differentiate because of their distinct courtship displays.
Once the pair is sexed, each fish can be distinguished utilizing the number and position of the silver-colored dots on their abdomens which have a specific pattern in each individual).
Signs of imminent spawning are an increase in the frequency of female approaches during side-by-side trembling, occasional trrembling and opening of the male's mouth, and the pair's proximity to the bottom. Egg release occurs when both individuals are situated side by side, separated about 1 to 2 cm and a few centimeters from the bottom. Occasionally, at the moment of the egg release, the male is located a few centimeters ahead of the female. When about 3/4 of the egg mass protrudes from the female's urogenital papilla (which takes between 1 and 1 1/2 seconds) the male immediately turns around and gulps the clutch by pulling the eggs from the female. The extraction of the eggs by the male requires some amount of pulling, and some eggs are cut off from the dutch and remain attached to the female for a few seconds until they fall off. Egg transfer is completed in no more than two seconds.
If the pair is kept with other specimens during the mating process, the mating female chooses and separates a receptive male :rom the rest of the school, and the pair establishes a home site that is aggressively defended. However, often a secondary male (SNMis allowed to intervene in the courtship. Unlike other approaching individuals, which are immediately chased, the SM is allowed to approach them. The SM follows the pair with a submissive posture, moves away from the pair, and maintains its distance when the pair swims in his direction. Then the SM participates in defense of the site, alone or with one member of the pair. The SM displays trembling behavior (rarely observed in the primary male, PM) and mouth opening to the female. If the PM responds to the female's displays (by remaining close to her and swimming to the bottom), the PM mates and takes the eggs while the SM does not intervene. However, if the PM does not show interest in the female's displays by swimming away and remaining at the middle-top section of the tank for extended periods), the female starts periodically leaving the PM and displaying mating behavior to the SM. The SM responds by swimming to the bottom, and frequently trembling. If the PM does not intervene, then the female occasionally mates with the SM.
Fecundity-Fertility
Considering the loss of some eggs during the egg-transfer and the normal mortality during embryo development, the expected fertility rate is about 60% (if the breeding pair is kept isolated under captive breeding conditions). If the brooding male is kept with other specimens during the incubation period, then he is usually under heavy stress due to harassment by the other individuals and by the stimulation at feeding time, with a consequent significant decrease of the fertility rate (generally, as spitting of eggs). Since the average number of mature ova before ovulation is about 60 oocytes, about 40 is the average number of juveniles released by an adult male. The highest observed number of released juveniles by one male in our lab was 62, and the highest frequency of deposition by a female observed was once every 25 to 30 days. Latest observations based on field specimens show that the reproductive cycle of P. kauderni has a lunar periodicity. Mating takes place during a few days preceding, during, and few days after full moon (preliminary data indicates that it also has a small reproductive peak duringthe new moon). The release of juveniles from the brooding male has the same periodicity.
Eggs
Ovulated oocytes measure between 2.7 and 3.0 mm in diameter. An average clutch consists of about 45 eggs that form a round mass 1.5 cm in diameter. The eggs are held together by strong filaments that originate on each egg's capsule and extend outward, entangling with filaments from other eggs. The eggs are ovoid and at spawning are bright yellow-orange with a yolk full of small lipid globules.
Embryos and Juveniles
Embryos hatch after 19 to 20 days of incubation at a postflexion state, and at 5.0 to 6.0 mm SL. Newly hatched eleutheroembryos (free embryos) have a large bilobed yolk and remain for a maximum of 10 days in the male's oral cavity, feeding endogenously until released. The release of most juveniles occurs between the 6th and 10th day after hatching, however, sometimes eleutheroembryos are expelled during the first few days. These premature juveniles are not capable of swimming and generally show signs of slow development. At release, juveniles are of 8 mm SL and their yolk is almost absorbed. Immediately after release, juveniles swim together forming a small compact school and are capable of eating items as large as Artemia nauplii. Observations from wild specimens agree with our lab studies in showing females maturing at about 35-36 mm SL, which corresponds to an approximately age of nine months.
Juvenile Requirement of a HUFA-enriched Diet for Normal Development
Studies in our lab have shown that during the first 3 to 4 months after release, juveniles are very susceptible to a deficit of highly unsaturated fatty acids (HUFA) in their diet. The lack of adequate HUFA intake produces a typical shock syndrome, characterized by sudden, extremely rapid, short, and jerky bursts of motion, brief spiral swims, and falling to the bottom with very expanded opercules and a considerable increase in ventilation frequency. Sometimes, juveniles slowly recuperate after a period of about 5 to 10 minutes. However, many suffer a very violent shock and die just a few seconds after falling to the bottom. This shock syndrome can be triggered by a moderate increase in stress, e.g., feeding, bumping on the tank, turning on the lights, etc. A HUFA-enriched diet reduces significantly the shock events, and decreases mortality to almost zero.
A simple method to deliver HUFA and a very efficient way to avoid the shock syndrome is to feed juveniles for the first three months with enriched newly hatched brine shrimp (Artemia sp.). During the first two months we feed juveniles with enriched Artemia (after hatching Artemia is enriched for 24 hours prior to feeding). After the second month, juveniles are fed a mix of enriched Artemia and very finely minced krill (Euphasia pacijica, E. superba) and mussels (Perna canaliculus). Older juveniles are fed adult Artemia (enriched with microalgae and HUFA supplement) and finely chopped krill and mussels.
Geographic Distribution and Ecology
Our work on geographic distribution included a survey of the entire Banggai Archipelago, the Sula Spur region, and in the area of central Sulawesi from Botok to Luk. In total we searched 86 sites localized in 37 Islands and two reefs. P. kauderni has a highly endemic natural distribution. The entire species is restricted to less than 10,000 km2. We found it off the following 16 islands: Banggai, Bakakang, Bangkulu, Bangko, Bokan, Labobo, Loisa, Masepe, Melilis, Peleng, Tempau, Limbo, Masoni, Mangoa, Seku, and Taliabu. Also, a small population inhabits Luwuk harbor in central Sulawesi. This population is restricted to a very small enclosure, the harbor itself, with very poor environmental conditions (besides daily spills of boat fuel, significant freshwater runoff, human waste, and all sorts of garbage are being dumped into the harbor).
In addition, a small (but growing), recently introduced population was found in the Lembeh Strait (North Sulawesi), approximately 400 km northwest of the Banggai Archipelago.
Habitat Preference
P. kauderni inhabits mainly protected bays on shallow reefs and seagrass beds. However, it also inhabits environments with strong surge and moderate currents. Its preferred depth range is between 0.5 and 4.5 m, but it is most commonly found between 1.5 and 2.5 m with water temperature ranging from 28° to 31°C (82° to 88°F). We found populations in very clear waters in coral reef areas associated with branching corals, while others inhabiting very still murky areas with very poor visibility. In several sites we found them in sandy patches associates with anemones, and on a few occasions in open habitats (low branching corals and rubble). We encountered about 60% of the groups living on coral reefs, 28% on sea grass beds, and about 12% on open areas of sand and or rubble.
The aim of this article is to bring to the hobbyist and aquarium community a summary of what is known to date about different aspects of the biology and conservation status of Pterapogon kauderni. In addition, I hope this review will help readers to appreciate its uniqueness among coral reef fishes, and will contribute to raising awareness with respect to the threatened status of its populations and habitat.
Introduction
The information presented here represents some of the results obtained during the last several years at the New Jersey State Aquarium (NJSA) in our research on the Banggai cardinalfish. The laboratory phase began in early 1997 and focuses on its reproductive biology, ecology, biogeography, evolution, and conservation, and included the development of a captive-breeding program. The fieldwork, which began in 2001 and continued in 2002, has been carried out in collaboration with Mark Erdmann (NRM/EPIQ, Sulawesi, Indonesia) and with financial support from the NJSA, The American Zoo and Aquarium Association (AZA), and The National Geographic Society.
For a detailed description on reproductive biology (including mating behavior, embryology, and juvenile development) see Vagelli (1999), for ecology and conservation see Allen (2000), Erdmann & Vagelli (2001), and Vagelli & Erdmann (2002).
BRIEF HISTORIC AND SYSTEMATIC REVIEW
The first time science learned of P. kauderni was in February 1920 when Walter Kaudern, during his 1917-1920 expedition to the Celebes Island (Sulawesi), collected two specimens close to the shore of Banggai Island and sent them to the Leiden Natural History Museum. Thirteen years later Frederick Koumans described the specimens as a new species and genus. He created the genus Pterapogon on the basis of the higher number of rays of the second dorsal fin, which distinguishes this genus from the rest of the apogonid genera.
In his 1972 work on Apogonidae, T. H. Fraser created the subgenus Pterapogon to differentiate the Banggai cardinalfish from Quinca mirifica, a cardinalfish from Northwestern Australia described by Mees in 1966, which Fraser classified within the genus Pterapogon (and subgenus Quinca). In November 1994 ichthyologist Gerald Allen and underwater photographer Roger Steen traveled to Banggai Island hoping to find this beautiful species, which fish guidebook author Kal Mullet had found in that area about two years earlier. In 1995 Allen and Steen published their observations on some ecological aspects of this species, and were the first to speculate about this species lacking a planktonic dispersal phase, and its connection with a very restricted geographical distribution. In 1997 the NJSA began a comprehensive research project on this species.
In 2000 a small population was detected in the Lembeh strait (North Sulawesi), the probable result of an accidental escape from holding nets that an exporter kept in that location.
Reproductive Biology
P. kauderni has a unique set of reproductive characteristics that makes it an exception among coral reef teleosts, e.g., it lacks a planktonic interval (its eggs do not enter into the plankton, and it lacks a larval period); therefore, this species does not have planktonic dispersal; it has very low fecundity; the male mouthbroods the egg-clutch for about 20 days, and after hatching, the embryos remain in the parent oral cavity for about 10 days until completion of development and release as juveniles. The brooding male does not eat during the entire incubating period, which lasts about 30 days.
PRESPAWNING BEHAVIOR
P. kauderni is a mouthbrooder in which transient pairs are formed and only the males incubate the eggs. Mating is preceded by an elaborate courtship that lasts normally several hours, but may extend to a few days. Prespawning behavior is composed of several courtship displays (female trembling, warping, side to side swimming, nuzzling and mouth-opening by the male).
The most characteristic prespawning display is the side-by-side trembling by the female (see Vagelli, 1999 for a detailed description of pre- and post-spawning behaviors). Side-by-side trembling normally lasts several hours. The only sign of a male's receptiveness is a conspicuous darkness along the lower jaw and sporadic mouth opening displays.
Spawning and Egg Transfer
P. kauderni reproduces all year long under laboratory conditions. Pair formation and courtship usually begin early in the morning and mating occurs during the first hours after noon. There is no secondary sexual dimorphism in this species. Therefore, the only method to differentiate sexes is to keep several individuals together and wait for the formation of pairs. Eventually, mature females will display an enlarged abdomen. Also, during pre-spawning behavior sexes are easy to differentiate because of their distinct courtship displays.
Once the pair is sexed, each fish can be distinguished utilizing the number and position of the silver-colored dots on their abdomens which have a specific pattern in each individual).
Signs of imminent spawning are an increase in the frequency of female approaches during side-by-side trembling, occasional trrembling and opening of the male's mouth, and the pair's proximity to the bottom. Egg release occurs when both individuals are situated side by side, separated about 1 to 2 cm and a few centimeters from the bottom. Occasionally, at the moment of the egg release, the male is located a few centimeters ahead of the female. When about 3/4 of the egg mass protrudes from the female's urogenital papilla (which takes between 1 and 1 1/2 seconds) the male immediately turns around and gulps the clutch by pulling the eggs from the female. The extraction of the eggs by the male requires some amount of pulling, and some eggs are cut off from the dutch and remain attached to the female for a few seconds until they fall off. Egg transfer is completed in no more than two seconds.
If the pair is kept with other specimens during the mating process, the mating female chooses and separates a receptive male :rom the rest of the school, and the pair establishes a home site that is aggressively defended. However, often a secondary male (SNMis allowed to intervene in the courtship. Unlike other approaching individuals, which are immediately chased, the SM is allowed to approach them. The SM follows the pair with a submissive posture, moves away from the pair, and maintains its distance when the pair swims in his direction. Then the SM participates in defense of the site, alone or with one member of the pair. The SM displays trembling behavior (rarely observed in the primary male, PM) and mouth opening to the female. If the PM responds to the female's displays (by remaining close to her and swimming to the bottom), the PM mates and takes the eggs while the SM does not intervene. However, if the PM does not show interest in the female's displays by swimming away and remaining at the middle-top section of the tank for extended periods), the female starts periodically leaving the PM and displaying mating behavior to the SM. The SM responds by swimming to the bottom, and frequently trembling. If the PM does not intervene, then the female occasionally mates with the SM.
Fecundity-Fertility
Considering the loss of some eggs during the egg-transfer and the normal mortality during embryo development, the expected fertility rate is about 60% (if the breeding pair is kept isolated under captive breeding conditions). If the brooding male is kept with other specimens during the incubation period, then he is usually under heavy stress due to harassment by the other individuals and by the stimulation at feeding time, with a consequent significant decrease of the fertility rate (generally, as spitting of eggs). Since the average number of mature ova before ovulation is about 60 oocytes, about 40 is the average number of juveniles released by an adult male. The highest observed number of released juveniles by one male in our lab was 62, and the highest frequency of deposition by a female observed was once every 25 to 30 days. Latest observations based on field specimens show that the reproductive cycle of P. kauderni has a lunar periodicity. Mating takes place during a few days preceding, during, and few days after full moon (preliminary data indicates that it also has a small reproductive peak duringthe new moon). The release of juveniles from the brooding male has the same periodicity.
Eggs
Ovulated oocytes measure between 2.7 and 3.0 mm in diameter. An average clutch consists of about 45 eggs that form a round mass 1.5 cm in diameter. The eggs are held together by strong filaments that originate on each egg's capsule and extend outward, entangling with filaments from other eggs. The eggs are ovoid and at spawning are bright yellow-orange with a yolk full of small lipid globules.
Embryos and Juveniles
Embryos hatch after 19 to 20 days of incubation at a postflexion state, and at 5.0 to 6.0 mm SL. Newly hatched eleutheroembryos (free embryos) have a large bilobed yolk and remain for a maximum of 10 days in the male's oral cavity, feeding endogenously until released. The release of most juveniles occurs between the 6th and 10th day after hatching, however, sometimes eleutheroembryos are expelled during the first few days. These premature juveniles are not capable of swimming and generally show signs of slow development. At release, juveniles are of 8 mm SL and their yolk is almost absorbed. Immediately after release, juveniles swim together forming a small compact school and are capable of eating items as large as Artemia nauplii. Observations from wild specimens agree with our lab studies in showing females maturing at about 35-36 mm SL, which corresponds to an approximately age of nine months.
Juvenile Requirement of a HUFA-enriched Diet for Normal Development
Studies in our lab have shown that during the first 3 to 4 months after release, juveniles are very susceptible to a deficit of highly unsaturated fatty acids (HUFA) in their diet. The lack of adequate HUFA intake produces a typical shock syndrome, characterized by sudden, extremely rapid, short, and jerky bursts of motion, brief spiral swims, and falling to the bottom with very expanded opercules and a considerable increase in ventilation frequency. Sometimes, juveniles slowly recuperate after a period of about 5 to 10 minutes. However, many suffer a very violent shock and die just a few seconds after falling to the bottom. This shock syndrome can be triggered by a moderate increase in stress, e.g., feeding, bumping on the tank, turning on the lights, etc. A HUFA-enriched diet reduces significantly the shock events, and decreases mortality to almost zero.
A simple method to deliver HUFA and a very efficient way to avoid the shock syndrome is to feed juveniles for the first three months with enriched newly hatched brine shrimp (Artemia sp.). During the first two months we feed juveniles with enriched Artemia (after hatching Artemia is enriched for 24 hours prior to feeding). After the second month, juveniles are fed a mix of enriched Artemia and very finely minced krill (Euphasia pacijica, E. superba) and mussels (Perna canaliculus). Older juveniles are fed adult Artemia (enriched with microalgae and HUFA supplement) and finely chopped krill and mussels.
Geographic Distribution and Ecology
Our work on geographic distribution included a survey of the entire Banggai Archipelago, the Sula Spur region, and in the area of central Sulawesi from Botok to Luk. In total we searched 86 sites localized in 37 Islands and two reefs. P. kauderni has a highly endemic natural distribution. The entire species is restricted to less than 10,000 km2. We found it off the following 16 islands: Banggai, Bakakang, Bangkulu, Bangko, Bokan, Labobo, Loisa, Masepe, Melilis, Peleng, Tempau, Limbo, Masoni, Mangoa, Seku, and Taliabu. Also, a small population inhabits Luwuk harbor in central Sulawesi. This population is restricted to a very small enclosure, the harbor itself, with very poor environmental conditions (besides daily spills of boat fuel, significant freshwater runoff, human waste, and all sorts of garbage are being dumped into the harbor).
In addition, a small (but growing), recently introduced population was found in the Lembeh Strait (North Sulawesi), approximately 400 km northwest of the Banggai Archipelago.
Habitat Preference
P. kauderni inhabits mainly protected bays on shallow reefs and seagrass beds. However, it also inhabits environments with strong surge and moderate currents. Its preferred depth range is between 0.5 and 4.5 m, but it is most commonly found between 1.5 and 2.5 m with water temperature ranging from 28° to 31°C (82° to 88°F). We found populations in very clear waters in coral reef areas associated with branching corals, while others inhabiting very still murky areas with very poor visibility. In several sites we found them in sandy patches associates with anemones, and on a few occasions in open habitats (low branching corals and rubble). We encountered about 60% of the groups living on coral reefs, 28% on sea grass beds, and about 12% on open areas of sand and or rubble.
