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Revealing the mysterious

Female Rough Ghost Pipefish, Solenostomus paegnius, in the wild. Can captive breeding domesticate desirable but impossible-to-keep species such as this?

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SCOTT WI. MICHAEL

by Richard Ross and Matt Wandell

Collec tion, husbandr y, and spawning of these enigmatic relatives of the seahorses and true pipefishes
Ghost Pipeshes are some of the most passed by andat the same time sought-after animals in tropical oceans. They are passed by because their cryptic nature and fantastic camouage make it likely that divers will not see them even when looking right at them; they are sought after because once you train your eyes to nd them, their beauty and visual extravagance is captivating.

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The Steinhart Aquariums male Solenostomus paradoxus behind the female, soon after their trip to San Francisco from the Philippines.

The track record of these intriguing and delicate shes in aquariums has been less than stellar. However, recent advances in the collection, husbandry, and display of hard to keep shes by aquarists the world over (and specically by our team of biologists at the Steinhart Aquarium in the California Academy of Sciences, San Francisco) may help to make not only the routine keeping, but also the captive breeding, of these amazing Ghost Pipeshes a reality. In the Pacic and Indian Oceans, Ghost Pipeshes are usually found individually or in male-female pairs, and rarely in trios of one female and two males. Their bodies often blend in perfectly with other organisms in their environment, making them very difcult to spot. The Robust Ghost Pipesh (Solenostomus cyanoptrus), the Delicate Ghost Pipesh (S. leptosoma), and the Longtailed Ghost Pipesh (S. armatus) have streamlined bodies and cryptic markings that let them hide in plain sight in and amongst patches of sea grass. As its name suggests, the shape and color of the body and ns of the Halimeda Ghost Pipesh (S. halimeda) make them indistinguishable from a clump of the green calcareous algae Halimeda. The most amboyant of the described Ghost Pipeshes is the well-named Ornate Ghost Pipesh (S. paradoxus), which is covered with myriad n rays and spines and is patterned to blend in perfectly with branches of gorgonians and black corals or among the arms of feather stars. Not to be forgotten is the rarely seen and currently un-

The first Solenostomus paradoxus and Solenostomus cyanopterus hybrid larvae on a metric rule graduated in millimeters.

Solenostomus paradoxus larvae at 6 days post-hatch.

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described Hairy Ghost Pipesh, which is covered in what look like ne hairs, presumably so that they can blend in with their environment.

RICHARD ROSS/CALIFORNIA ACADEMY OF SCEINCES

F I N N AG E, S E X , A N D LO N G E V I T Y Ghost Pipeshes are found in the Order Syngnathiformes, which includes familiar seahorses and pipeshes (Syngnathidae), as well as some other closely related families such as the trumpetshes (Aulostomidae), cornetshes (Fistulariidae), shrimpshes (Centriscidae) and sea moths (Pegasidae). The ve described species of Ghost Pipeshes are not true Syngnathids like seahorses, but occupy their own family, the Solenostomidae. One of the key differences that distinguish Solenostomids from the Syngnathids is that Ghost Pipeshes possess pelvic ns, and seahorses and pipeshes do not. The pelvic ns of the Ghost Pipeshes actually play a key role in their unique reproductive strategy. Many people are familiar with the way male seahorses become pregnant by carrying the eggs in a pouch near their abdomen until they hatch. In Ghost Pipeshes, the male provides sperm while the female carries the eggs in her large, modied pelvic ns until they are ready to hatch and she ejects them into the ocean with a ick of her ns. Distinguishing between the sexes is simple: Females can be nearly twice as large as males, and the pelvic ns of females are greatly enlarged to create a cavity where she holds her eggs. A female carrying eggs is relatively easy to spot, because her pelvic ns gently undulate like a bellows to create a current that washes over the eggs inside. We have not been able to nd any studies on wild longevity of Ghost Pipeshes, but accounts by dive operators indicate that these shes are seasonal and appear on the reefs as adults for only about half of the year. This suggests that they have very short life spans, perhaps only a year, and the sudden appearance of individuals on the reefs every year coincides with the metamorphosis of the previous years offspring from planktonic larvae to benthic adult sh. Captive experience with Ghost Pipeshes also suggests a short life span; even the very rare individuals that adapt to captivity live only a few months before dying for no apparent reason. I M P O S S I B L E TO K E E P ? The overwhelming consensus among saltwater aquarium keepers is that Ghost Pipeshes are impossible to keep in captivity. Over the years we have developed a healthy sense of skepticism when it comes to the old warnings about animals that should simply be left in the ocean. This skepti-

cism stems from an understanding that much of the time these animals are simply not given the specialized care they need to survive. Of course a shy, difcult-to-feed sh placed in a well-stocked reef aquarium will fail to thrive. However, recent work with the Orangespot or Harlequin Filesh (Oxymonocanthus longistrosis), Purple Queen Anthias (Psuedanthias tuka), octopus, cuttlesh, Acropora, and a whole host of non-photosynthetic corals has shown that, although they require a bit of specialized work, these once seemingly impossible animals can not only live but thrive, and sometimes even reproduce in captivity. Why should the Ghost Pipeshes be any different? There are three criteria needed for success with difcult to keep animals, though satisfying all three can be easier said than done. 1) A low-stress environment where tankmates, swimming room, hiding space, temperature, and lighting are all carefully considered and developed. 2) An abundant supply of a food that the animal will actually eat, that satises its nutritional requirements, and that is fed often enough to allow for the animals biological needs.

A peek into the modified ventral fins of the female Solenostomus paradoxus reveals eggs and larvae at different stages of development.

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Ornate Ghost Pipefish, Solenostomus paradoxus, wild male.

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Ornate Ghost Pipefish, Solenostomus paradoxus, pair (larger female, left).

3) Starting with a healthy animal that hasnt been overstressed by its journey from the ocean to aquarium life.

F E E D I N G D E M A N D S TO P O N D E R As it turns out, for Ghost Pipeshes, satisfying the rst two requirements are fairly straightforward. Ghost Pipeshes will do perfectly well in the light, ow, temperature, and space in various styles of low- to mid-energy 30- to 40-gallon (113151-L) coral reef aquariums. A high-energy, SPS-style reef tank is not appropriate. While probably ideally kept in a species-only display, they may cohabitate with mellow tankmates. Ghost Pipeshes will readily eat live mysid shrimp, which can be cultured, collected, or purchased. It is important to note that the need for live mysids will be a deal-breaker for most people interested in keeping Ghost Pipeshes, because feeding live mysid shrimp can quickly become expensive. We believe that this is where responsible husbandry on

the part of the aquarist comes into play, and we urge anyone interested in keeping Ghost Pipeshes (or any other hard to keep animal) to be sure they can provide what we know the animals need to survive. Trying to obtain Ghost Pipeshes without being able to supply live mysids, even while experimenting with other foods, seems irresponsible. As with many difcult to keep animals, the trick is obtaining a healthy specimen in the rst place. Ghost Pipeshes (and many difcult to keep animals) seem incredibly sensitive to the stresses involved in shipping and collection. Many wholesalers refuse to even entertain the idea of ordering them anymore because when the shipment arrives, the frequent result is a very beautiful, but very dead sh. Unfortunately, the stresses of capture and handling that most marine shes endure in the chain of custody to make it from a coral reef in the South Pacic or Indian Ocean to a home aquarium in the U.S. are often too much for Ghost Pipeshes to live through. A several-weeks-long journey, during which a sh moves through the holding tanks of multiple collectors, exporters, wholesalers, and retailers, is bagged and re-bagged, and is fed sparsely or not at all, is almost certainly the cause of stress and death for most Ghost Pipeshes. In other words, delicate shes need special handling and care that the traditional aquarium chain of custody, focused on economies of scale, generally does not provide. In an ideal world, we would be able to personally, carefully hand-catch our precious cargo of healthy Ghost Pipesh, transport them immediately after collection in large containers where water quality and temperature are carefully controlled, and get them on a plane to their nal destination within a day or two after collection. Sounds like a pipe dream, right? Not necessarily.

CO L L E C T O U R OW N? R E A L LY? In the spring of 2011, we found ourselves diving the reefs of Anilao in Southern Luzon, Philippines, as part of the California Academy of Sciences 2011 Philippine Biodiversity Expeditionthe largest expedition in the 90-year history of the Academy. During the expedition, a team of American and Philippine scientists, divers, and aquarium biologists surveyed several reefs and discovered and catalogued between 300 and 500 new species of shes and invertebrates. The beauty of this expedition was the combination of research and aquarium science. Part of the scientic process of identifying and describing new species is the requirement that live speci-

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S M A L L - S C A L E M YS I S S H R I M P C U LT U R E Anyone thinking about attempting to keep Ghost Pipeshes will need a consistent live food source, and it should be in place before the sh arrive. Live mysid shrimp are known to elicit a feeding response and provide proper longterm nutrition in Ghost Pipeshes. Unfortunately, mysids are considerably more difcult to provide in large numbers than common staples like live brine shrimp or Daphnia. It takes quite a bit of time or expense, or both, to provide enough live mysids to satisfy the diet of Ghost Pipeshes. A small male can be expected to eat 10 live mysids per day, but a large brooding female may require 50 or more per day. A suitable species of mysid for feeding to these shes is Americamysis bahia (formerly Mysidopsis bahia). This species is found along the Gulf of Mexico and Florida coasts, in estuarine and coastal waters, and is commercially aquacultured in large numbers for aquatic toxicity testing. In captivity they can be held at 1535 ppt salinity and 7080F (2127C). Dedicated aquarists can culture this and other species of mysids at home. One common strategy for mysid culturing is to house a low density of adults in several 1020-gallon (3876-L) tanks and let the water ow down through an overow drain to a common sump housing the life support. The drains are screened with 1-mm (25-m) mesh so that juveniles will pass through but the adults wont. Before entering the sump, a nely screened (300-m) bas-

ket catches the juveniles where they can be removed and fed out daily or grown out to a larger size. Mysid cultures require quite a bit of space and effort to function properly. Aquarists lucky enough to live near a coast can almost certainly nd a bay, estuary, or harbor where mysids are found in abundance and can be collected. The simplest way to collect them is to troll the water surface at night, when they make a nightly vertical migration in search of food. If you dont live near a coast, dont give up hope just yet many inland freshwater lakes have thriving populations of mysids as well. Before actually collecting any mysids, be sure to check with your local and state laws to verify what you are doing is legal. Another option for those who would rather spend money than time acquiring live mysids is simply to purchase them. Many aquaculture companies collect or culture Americamysis bahia and other species and will ship them directly to your door. Currently, you can expect to pay somewhere in the neighborhood of $80 for 500 wildcollected mysids, plus shipping. Whether you collect, purchase, or culture your mysids, they will need a place to stay until they are fed out to your Ghost Pipeshes. If they are held in high densities, mysids can cannibalize each other, and poor water quality may cause the culture to crash, so consider plumbing the mysid holding tank into a larger system if possible. Low-density mysid populations, on the other hand, are not difcult to maintain and can be ltered with simple air-driven sponge lters. Ghost Pipeshes are what they eat, so feeding your mysids a well-balanced diet is very important. Mysid shrimp will consume just about any edible material that is of the correct size, so nely crushed ake and pellet foods make suitable foods, as well as live Artemia nauplii or rotifers.
ON THE INTERNET

MBL Aquaculture, source for live Americamysis bahia: www.mblaquaculture.com/content/organisms/ americamysis_bahia.php EPA Culture Manual for Mysidopsis bahia: nepis.epa.gov/Exe/ZyPURL.cgi?Dockey=910057BH.txt
Mysis shrimp, the ideal live food for Syngnathiformes, cultured at the California Academy of Sciences.

mens are collected and preserved for future study. This turned out to be a win-win for aquarium biologists, as we got to work with animals we would normally not be able to work with. Instead of immediately preserving animals for later research, we rst cared for them in a captive setting to learn about their behavior and biol-

F R O M T H E P H I L I P P I N E S TO S A N F R A N C I S CO The animals were collected and packed for shipping with great care. The sh were hand-collected with plastic bags

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RICHARD ROSS/CALIFORNIA ACAADEMY OF SCIENCES

ogy, allowing them to live out their lifespans before becoming valuable preserved specimens. This process gave us the unique opportunity to care for several Ghost Pipeshes from the moment they were hand-collected in the wild until they were added to small reef aquariums on public display at the Steinhart Aquarium.

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Female Ornate Ghost Pipefish, Solenostomus paradoxus, with eggs.

and immediately carried up to waiting boats and transported to the holding area, to be shipped to San Francisco as soon as possible. Ghost Pipefishes have been known to gulp, or pipe, air into their bodies during shipping, making them float at the waters surface, which can cause their death. To avoid this potential problem we bubbled oxygen through the shipping water and packed the bags with between 10 and 20 percent air, as well as further protecting the animals in their own rigid container (often sold under the brand name Kritter Keepers) within the shipping bag to keep them away from the waters surface. Each individual was shipped in a large bag with approximately 1 gallon (3.78 L) of sea water. Fish that were collected on one day, kept on land in

their own 5-gallon (18.9-L) buckets with 100 percent water changes every 4 hours, and shipped the next day had a 100 percent survival rate; collection-to-tank times were less than 36 hours. Animals that had collection-totank times of over 48 hours did poorly. It is our belief that shipping immediately after capture, in large, bags where the fish have no access to air, is essential to their survival in the shipping process.

G H O S T P I P E F I S H E S O N D I S P L AY In San Francisco, the aquarium staff was excited to receive a thriving pair of Solenostomus paradoxus and a large female Solenostomus cyanopterus. The decision was made to put all three animals directly on display in established aquariums in order to mitigate stressors and give them

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Pair of Rough Ghost Pipefish, Solenostomus paegnius, smaller male in foreground.

access to the potential food sources naturally occurring in mature tanks. The female S. cyanopterus went into our calm feather duster exhibit, while the pair of S. paradoxus went into the larger and more energetic Dwarf Cardinal (Apogon parvulus) and soft coral exhibit. Both of these exhibits were tied into larger systems, so water quality and stability were maximized. The Ghost Pipeshes seemed to become conditioned to aquarium life very quickly, hiding in plain sight alongside corals on exhibit and not showing any signs of obvious stress, to the delight of guests. Almost immediately the females began eating live mysids offered in both the morning and evening, which quickly turned into four or ve times per day to make sure the sh received the food they needed. In general the tank was ooded with so many live mysids that the shes could spend several hours per day hunting them. To maximize the nutritional punch, live mysids were fed twice daily with 48-hour Artemia nauplii, Otohime brand size A pellets, and crushed ake food. The male S. paradoxus did not eat with as much gusto as the females, which could be attributed to his smaller size, but he was seen to eat on several occasions and continued to grow. Thawed frozen Hikari and Piscine Energetics brand mysids and live adult Artemia were offered from time to time, but none of the sh ever showed any interest. Another potential food source in captivity are small feeder sh; large Ghost Pipeshes are known to hunt and consume very small shes in the wild, and some are reported to feed on live guppies in captivity as well. However, the nutritional implications of feeding Ghost Pipeshes a diet solely composed of freshwater sh is unknown, so we did not pursue that course of action. In our experience a diet composed solely of enriched live mysid shrimp is suitable for Ghost Pipesh survival, growth, and, to our surprise and amazement, even reproduction.

E G G S A N D M AT I N G Within days of our return from the eld it was discovered that both of the female Ghost Pipeshes were apparently collected already holding eggs. Even though the female S. paradoxus was already gravid, the pair were observed mating nearly every morning. We watched eagerly as we caught glimpses of developing eyes between n beats for the next two weeks when overnight, some, but not all, of the larvae were released in the S. paradoxus aquarium. The larvae were collected but quickly perished, presumably from handling stress. It was also noted that several live mysid shrimp were able to catch and kill the tiny larvae. After discussions with sh breeder Tom Verhoeven, we decided on a plan to bring the female to the larval rearing tank to release her larvae rather than trying to catch them in a display full of corals. Each night over the next three consecutive nights, the female S. paradoxus was isolated in a large kreisel tank, where she released larvae; every morning, when she was placed back with the male, they would mate within less than a minute. The fourth night in isolation produced no larvae. Shortly after this we were able to share some of the rst video of Ornate Ghost Pipeshes (S. paradoxus) mating in captivity at the Steinhart Aquarium (see references at the end of this article). Mating in Ghost Pipeshes consists of the male approaching the female with his ventral side facing hers and his body oriented at a 90-degree angle to hers, to allow access to the egg cavity in her pelvic ns. When the female is ready she opens her pelvic ns wider than usual and the male trembles for a few seconds as he releases sperm. After mating the female keeps the pelvic ns clamped shut, but splays out the n rays repeatedly in the dorsal/ventral plane for several minutes. This is an entirely different motion than the one she uses to gently aerate the eggs by pumping her pelvic ns like a bellows,

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and is presumably a way to ensure that all her eggs are fertilized by the males sperm. Over the next three months we were able to collect larvae three times and raise them to about 15 days by adding L-strain rotifers, Parvocalanus sp. copepods, Nannochloropsis sp. phytoplankton, and Shellsh Diet phytoplankton blend, all from Reef Nutrition. Based on our observations in captivity, a female Ghost Pipesh can carry several rounds of eggs and larvae at varying stages of development. Hatching and ejection from the safety of the pelvic ns was observed to occur for 37 days at 23 week intervals. If given the opportunity, at least one species of Solenostomus (S. paradoxus) will mate and release larvae every 24 hours, usually at dawn. Because of this pattern, it is very difcult to ascertain exactly how long larvae take to develop from a fertilized egg to larvae ready to be released. Our experience indicates that the drive to reproduce in these shes is very strong; male-female pairs of Ghost Pipeshes are certainly not hesitant to get it on even when they have been released from a bag just moments earlier. After about 6 months in captivity, we lost the female S. paradoxus. As mentioned previously, this may be an annual sh, implying a naturally short lifespan of only 912 months in the wild. Given that the female was large when she was collected, we were proud to have kept her alive and reproducing for at least her natural lifespan. Unfortunately, her passing left us with a male of one species of Ghost Pipesh and a female of another. So, hoping that they might make good company for each other, we put the two sh together in the same tank. It was jokingly suggested that they might even mate, despite being of separate species, but the Ghost Pipeshes took our suggestion to heart. Despite initially mostly ignoring each other, the two began to show courtship behavior and eventually began to carry and fertilize eggs regularly. It should be noted that, while we thought the female S. cyanopterus had been producing eggs, none of them, with the possible exception of the batch she was collected with, were ever fertileun-

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til the spawning with the male S. paradoxus began. This gravid female was isolated as the S. paradoxus female had been, but in a round, black tub instead of a kreisel tank. Amazingly, we were able to raise these hybrid Solenostomus (cyanopterus X paradoxus) larvae to 22 days on the same co-culture of rotifers, copepods, and phytoplankton. Ghost Pipefishes are beautiful and captivating animals, and it is our opinion that if collected carefully and shipped well and quickly, that they are potentially a prime candidate for successful captive breeding. That said, we feel it would be horrible if there was a spike in demand for these animals before the shipping is worked out (which will also rightfully increase the retail cost of Ghost Pipefishes) and successful shipping becomes commonplace. Premature growth in imports would result in the deaths of many fishes. It would be even worse if people obtained these animals without taking steps to provide the calm conditions and live foods needed for their aquarium survival. We now know more about Ghost Pipefishes than we did before, but keeping them alive in the aquarium

is currently difficult, time consuming, and expensive, and its not an endeavor to be entered into lightly. It is our hope that the Steinhart Aquarium in the California Academy of Sciences will be able to continue to work with these fantastic fishes in the near future.
REFERENCES:

Fishelson, L. 1966. Solenostomus cyanopterus in Elat (Gulf of Akaba). Israel J Zool 15: 95103. Kimura, S. and Sado, T. 2006. Descriptive morphology of yolk sac larval Solenostomus paradoxus collected from Libong Island, Trang, southern Thailand. Ichthyol Res 53 (2): 18991. Wetzel, J. and Wourms, J.P. 1995. Adaptations for reproduction and development in the skin brooding ghost pipefishes, Solenostomus. Env Biol Fishes 44 (4): 36384. Verhoeven, Tom. Pers. comm.
ON THE INTERNET

Steinhart Aquarium video of Ornate Ghost Pipefish mating and releasing larvae: www.advancedaquarist.com/blog/twospecies-of-ghost-pipefish-spawn-and-produce-larvae www.advancedaquarist.com/blog/ornate-ghost-pipefishmating-releasing-larvae-caught-on-video

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