Does Anybody Really Know What Time It Is? Lamprey Do! by Don Orth

We humans are obsessed about time. Our lives are structured around time.  We take time management workshops with a false belief that we can manage time.  Yet, we can only manage to prioritize activities, not time. My alarm rings at 6:00am, I fail to notice a sunrise at 6:29am, eat, shower, start my commute (clock in my car reads 7:34am), arrive to many auto-scheduled emails, approve time sheets, grade assignments, impose late submission penalties, attend committee meeting at 10:00am, arrive to class at 12:20pm, dismiss class promptly at 1:10pm, and the whole day is scheduled like that. The sun sets at 8:06pm and I might ponder the peculiar nature of time in our modern world.  Our obsession with time has a very long evolutionary history that is evident in all animals.

The lyrics from The Chicago Transit Authority’s hit song, “Does Anybody Really Know What Time It Is?” (1969), questions this obsession with time

“As I was walking down the street one day
A man came up to me and asked me what the time was that was
On my watch, yeah
And I said
Does anybody really know what time it is
I don't
Does anybody really care
If so I can't imagine why
About time
We've all got time enough to cry”

The song is about caring, the human condition, and human emotions.  The song was written at a time when many soldiers were dying in Viet Nam and yet the rich and privileged appeared to be unconcerned.   Listen here.  Humans care too much about time,  and not enough about things that matter.  Fish, on the other hand, live their lives with an internal clock that controls timing of biological processes.   

           

Deep within our brain sits a very small endocrine gland called the pineal gland.  It's the size of a pea, and this tiny pineal gland  secretes the melatonin.  Melatonin is a hormone that helps regulate human sleep and wake cycles.  When light hits the retina, a message is sent to your hypothalamus, and nerve fibers transmit this message down the spinal cord to sympathetic nerve cells that then ascend back up to the pineal gland.  Message is received and melatonin secretion ceases.   It’s time to wake up!

In the fishes, a very similar mechanism is at work to allow a fish to track changes in day length and time development and maturation of the gonads. Fish, like other animals, secrete melatonin at night and exhibit circadian rhythms.  Melatonin levels regulate activity of fishes.  Nocturnal fishes became active when melatonin levels increase, whereas diurnal fishes become active when melatonin levels are low.  Fish do not sleep in the same way humans do.  For one thing, they have no eyelids so the eye remains open.  Metabolism and behaviors slow, but they don’t appear to have deep sleep REM cycles (Laming 1981).

Hagfishes and the lampreys, the most primitive fishes, have the capacity to detect light and dark.  Hagfish have no eyes and no pineal gland, but do possess primitive photoreceptors that have nerve connections to brain.  The lamprey eye develops slowly during larval stage, but is functional early in life.  Lampreys also have a pineal gland at the top of head above brain.  The tissue overlying the pineal gland is transparent in the larval stage and translucent in the adult.  It appears the photosensitive pineal functions in an analogous manner as the retina photoreceptors in the human. The molecular mechanisms are the subject of ongoing studies of evolution of vertebrate photoreceptors (Mano and Fukada 2007) and the pervasive influence of circadian rhythms.  The blind Mexican tetra has been cut off from cues of the rising and setting sun; it has no circadian rhythms. 

Parapinopsin (A) and rhodopsin (B) pigments are expressed in different regions of photoreceptor cells   Photo from Koyanagi et al. (2004).  P=pineal, PP=parapineal, L=lumen, and S=pineal stalk.  (Scale bar=100 μm) Source

In the lamprey, the pineal gland has two components, a pineal (upper gland in photo) and a parapineal (lower gland in photo).  Each has two parts with UV and visible light sensitive regions. Research on the lamprey pineal gland confirmed that visible light excites the pineal, while UV light inhibits the pineal response (Koyanagi et al. 2004).  Therefore, the lamprey really do know what time it is!  

Zebrafish is a valuable vertebrate model due to fast development, short generation time, and a large number of embryos.  Consequently, they are frequent subjects for the study of the circadian clock and the pineal gland.  The pineal gland develops early in the zebrafish, is photoreceptive and contains an intrinsic circadian oscillator that controls many physiological and behavioral processes.   

Location of pineal gland in zebrafish (top) and zebrafish embryo. Photos by Yoav Gothilf

Zebrafish have a gene, aanate (or for a long version, that would be aralkylamine-N-acetyltransferase), that exhibits clock-controlled rhythms (Gothilf et al. 1999).  Imagine a gene that is light sensitive; light is mandatory to set the circadian clock in zebrafish.  The gene exists in every cell allowing for the study of this “clock gene” in zebrafish cell lines (Vallone et al. 2005). The clock gene has a circadian rhythm in gene expression, which translates to circadian rhythms in metabolism and behavior in the zebrafish. 

What does this mean to the practicing fish worker?  Circadian rhythms in fish are established by the prevailing day/night cycles.  Maintenance of the circadian rhythms is important to the well-being of fish.  It is possible to control photo and thermal cycles and reduce the time needed for reproductive maturation in captive, farmed fish (Blythe et al. 1994). Alternatively, hormone injections may advance gonadal development.  Light and dark cycles and feeding times can also be controlled to optimize growth and survival of fish in captivity.  Fish are also great subjects for school science projects.  Novice scientists can observe the daily activity patterns of fish in an aquarium and experiment with changing time of day when lights are turned on.  They study fish!  They become more curious! They begin to contemplate life!  They begin to really know what matters!

References

Blythe, W.G., L.A. Helfrich, and G. Libey. 1994. Induced maturation of striped bass (Morone saxatilis) exposed to 6-, 9-, and 12-month photothermal regimes.  Journal of the World Aquaculture Society 25:183-192.

Gothilf, Y, et al. 1999. Zebrafish serotonin N-acetyltransferase-2: marker for development of pineal photoreceptors and circadian clock function. Endocrinology 140:4895-4903.  

Koyanagi, M., et al.  2004. Bistable UV pigment in the lamprey pineal. Proceedings of the National Academy of Sciences 101:6687-669. 

Laming, P.R. 1981.  Brain mechanisms of behaviour in lower vertebrates.  (Society for Experimental Biology Seminar Series).  Cambridge University Press, Oxford.  332 pp.

Mano, H., and Y. Fukada. 2007.  A median third eye: pineal gland retraces evolution of vertebrate photoreceptive organs.  Photochemistry and Photobiology 83(1):11-18.  DOI: 10.1562/2006-02-24-IR-813.  

Noche, R.R., P.N. Lu, L. Goldstein-Kral, E. Glasgow, and J.O. Liang. 2011. Circadian rhythms in the pineal organ persist in zebrafish larvae that lack ventral brain. BMC Neurosciences 12:7. DOI:10.1186/1471-2202-12-7.    

Vallone, D., K. Lahiri, T. Dickmeis, and N.S. Foulkes. 2005.  Zebrafish cell clocks feel the heat and see the light! Zebrafish 2(3):171-187. DOI: 10.1089/zeb.2005.2.171   

The Social Network and the Sand Tiger Shark, by Don Orth

Long before the movie, The Social Network, scientists have been investigating social networks – first in humans and, more recently, in wild animals.  A social network is a group of individuals interconnected by social ties between them; these interactions may be sexual, cooperative, learning, disease transmission, or others (Krause et al. 2015). Understanding the social network structure provides insights that the study of simpler, two-individual interactions cannot provide. Recently, a press release highlighted the social network of the Sand Tiger Shark Carcharias taurus (Carchariniformes; Odontaspididae). 

Most applications of social network theory to the study of animals have focused on more easily observable subjects, such as captive mammals, so this work on a free-living fish is innovative. Danielle Haulsee and her colleagues tracked 300 Sand Tiger Sharks over a one-year period, in order to provide the first evidence that this apex predator displays a more complex social structure than previously thought. The same research team had described the habitat selectivity of migrating Sand Tiger Sharks with acoustic telemetry and an autonomous underwater vehicle. Therefore, they knew where this coastal shark was migrating, but understanding their social network is a more challenging problem. In order to solve the first problem of obtaining behavioral data on a large mobile predator in the open ocean, the investigators used archival tags that recorded detections from nearby telemetered animals.  

Sand Tiger Shark amidst shoal of prey fish. Photo by  Tanya Houppermans/Caters News Agency

The Sand Tiger Shark is one of the best-studied sharks, and, therefore, a good fish to begin to examine social networks.  Populations are concentrated along the mid Atlantic coast and uncertainty over population declines prompted NOAA to continue to list the Sand Tiger Sharks as a species of concern.   Their low net reproductive rate means the populations will be slow to recover after prohibition of harvest by commercial and recreational fisheries in 2006.   

 

Close up of head of Sand Tiger Shark. Photo National Aquarium.

One look at the mouth of a Sand Tiger Sharks will tell you this fish is a specialized piscivore.  Consequently they are frequently captured by recreational anglers as well as longline and gill net fisheries.  Pioneer shark-watcher, Russell J. Cole, observed schools of Sand Tiger Sharks surrounding and herding schooling prey in order to feed on them. The systematic and coordinated movement of hundreds of Sand Tiger Sharks has the hallmarks of cooperative feeding behavior, a phenomenon more associated with dolphins and birds.        

Close up of teeth of Sand Tiger Shark.  Photo from National Aquarium.

 

While most sharks provide buoyancy with a large liver, the Sand Tiger Sharks also gulp air at the surface and store it in their stomach to provide buoyancy. These sharks generally mate in the fall after a courtship that involves the male aggressively nipping his potential mate.  Females give birth to only one or two large pups every two years and gestation lasts for nine months. Pups hatch and develop in the female.  By the time they reach 17 cm, they already possess prominent teeth and feed on new eggs and embryos produced by the female, a form of nutrition called ovophagy and embryophagy.  It’s hard to say how many eggs are eaten before the pups are born at a size of almost one meter.   Demian Chapman and colleagues did genetic tests on embryos in the uterus of a number of Sand Tiger Sharks.  As expected, the females mated with multiple males, but 60% of the females were carrying only babies from the same father.  Perhaps females have multiple mates in order to feed the offspring from the first father.  For the Sand Tiger Shark, the uterus is a safe place from predation from other sharks, however, it is not a safe place from being cannibalized by your sibling womb-mates.

Small and embryos from same uterus of Sand Tiger Shark. Photo by D.L Ambercrombie

Social networks are of interest to scientists studying social animals; social animals have a variety of strategies that individual animals use in groups. How can scientists understand how cooperation, aggression, information flow or dominance at the individual level translates to group phenomenon? Animals are not robots whose behavior is programmed by genes; rather they are individuals and their behavior is influenced by genetics, the environment, and social interactions.  Animals learn and they remember.   The group, or the network, is also important since information flows between some members in the group.  Social network analysis is needed to understand processes such as pathogen transport, feeding, movements, mating opportunities, and teaching survival skills.  Importantly, certain individuals play a larger role in the well-being of the group (Dugatkin and Hasenjager 2015).

The social network methods originated largely from psychologists and anthropologists.  For a brief history, click here. Scientists today study groups of individuals and monitor the many types of individual interactions in order to provide a network of social structure.  For example, which individuals are more likely to be affiliated in space or time and which individuals are avoided, or pursued as mates?  Although there are many applications, the analysis of social networks permits scientists to investigate the role of individual variation in social behavior on population structure.  Sophisticated methods for analyzing social networks are emerging.  These novel methods allow for  the study of networks of genetic, affiliative, agonistic, cooperative, dominant, and other relationships that form the social system (Wey et al. 2008; Farine and Whitehead 2015)

Social networks are most studied in social mammals, such as dolphin  (Lusseau and Newman 2004), bats, and other mammals, such as Zebras.  Social networks have also be applied to explore how the information-sharing networks contribute to fishing success in the Northumberland lobster fishery (Turner et al. 2014). Why should we study social networks?  The new investigation of the Sand Tiger Shark tells us that there is much more to learn about fish in social networks.  Social networks matter in contributing to the well-being of the group.  We need to consider the possibilities and open our minds to study possibilities of these hidden networks. 

References

Chapman, D.D., S.P. Wintner, D.L. Abercrombie, J. Ashe, A.M. Bernard, M.S. Shivji, and K.A. Feldheim. 2013.  The behavioral and genetic mating system of the sand tiger shark, Carcharias taurus, an intrauterine cannibal.  Biology Letters.   

Dugatkin, L.A., and M. Hasenjager. 2015.  The networked animal.  Scientific American 312:50-55.   

Farine, D.R., and H. Whitehead. 2015. Constructing, conducting and interpreting animal social network analysis.  Journal of Animal Ecology 84:1144-1163.

Lusseau, D., and M.E.J. Newman.  2004.  Identifying the role that animals play in their social networks.  Proceedings of the Royal Society of London B (Supplement) 271:S477-S481.  DOI 10.1098/rsbl.2004.0225

Krause, J., R. James, D.W. Franks, and D.P. Croft, editors.  2015. Animal social networks.  Oxford University Press.  Oxford, United Kingdom.  288 pp.

Turner, R.A., N.V.C. Polunin, and S.M. Stead. 2014.  Social networks and fishers’ behavior: exploring the links between information flow and fishing success in the Northumberland lobster fishery.  Ecology and Society 19(2):38.  

Wey, T., D.T. Blumstein, W. Shen and F Jordan.  2008.  Social network analysis of animal behaviour: a promising tool for the study of sociality. Animal Behaviour 75:333-344.  

Asian Arowana "The Fish of Paradise" by Don Orth

Water monkeys that

Will outgrow aquaria

Do not buy or sell!

The Asian Arowana Scleropages formosus (Müller & Schlegel, 1844) is also known as the Golden Dragonfish or Golden Arowana.  In the Indonesian language, arowana means “the fish of paradise.”  However, this prized symbol of feng shui, has been driven towards extinction.   It lives in flooded forests, swamps, and sluggish rivers at very low densities throughout its range in southeast Asia.  Low densities are largely due to poaching in the international aquarium trade, draining swamp habitats for agriculture, and logging swamp forests. 

Asian Arowana Scleropages formosus

Asian Arowana are captured by subsistence fishers, who seldom eat them.  Rather they keep it alive to sell the fish for aquarium trade.  Trade of the Asian Arowana is restricted, but the fish is so highly valued that wild-caught specimens are frequently illegally sold.

Why its illegal to sell this fish?   Asian Arowana are endangered under the Convention on Trade in Endangered Species (CITES) and the US Endangered Species Act.  Breeders in Indonesia and Malaysia must be licensed and registered with the CITES Secretariat.  Each Asian Arowana that is exported must be microchipped and proof of certification must follow a process approved by CITES.  In order to import an Asian Arowana, you would need a permit from the US Fish and Wildlife Service, in order to justify your use.  Leave that to the large, pubic aquariums.  Asian Arowana may live for many decades and require very large aquaria (many hundreds of gallons) in order to thrive.    A San Diego man was convicted of illegally importing Asian Arowana and others are frequently prosecuted over illegal trade in arowanas. 

Asian Arowana are specialized surface feeders with a large mouth  and eyes that have binocular vision.  They can eat any type of fish. The tip of the lower jaw has large protruding barbels that are filled with taste buds.  The sensory barbels aid in feeding in murky waters. They are also able to leap from the water to capture insects and spiders.  Examination of their guts indicates they sometimes eat birds, bats, and snakes. This leaping behavior explains the name “water monkeys.”   Warm swamps or sluggish rivers with frequent periods of low oxygen are favored habitats of the Asian Arowana, which are facultative air breathers.  They have vascular tissues in swim bladder.

Asian Arowana (close up of head) showing the large protruding sensory barbels. Photo by Marcel Burkhard (Creative Commons)

This beautiful fish will be difficult restore to its native habitats due to pervasive habitat changes in southeast Asia (Koh et al. 2013).  The Freshwater Fisheries Research Station (FFRC) in Malaysia successfully bred the Golden Arowana in captivity in 1996.  During courtship the male chases the female and sometimes the pair swims together in a circle.  The pair eventually swim side by side with bodies touching, and the female releases a cluster of large, reddish orange eggs that are immediately fertilized by the male.   But the male’s parental role is not over yet.  The male scoops up the fertilized eggs into his mouth, where he incubates them until fry hatch and can swim independently.   The mouth-brooding male is busy with these chores for about 8 weeks. 

Arowana fry being released from mouth of parental male.  Photo source.

In wild populations, the color is usually silver with hints of red, gold, green, black, and/or blue. Colors vary among differing populations of Asian Arowana, as some populations became more isolated after sea levels rose in the Pleistocene.  Breeders cross varieties and create different colors in Asian Arowana, in particular the vibrant reds and golds that are most desired.    Recently, a team of scientists sequenced the genome of the Asian Arowana and identified 94 genes that may influence the color patterns (Austin et al. 2015). 

Young Asian Arowana in the mouth of parental male.  Source.

The Asian Arowana is a part of a very old lineage of early bony fishes that arose on the ancient supercontinent of Gondwana, which broke up 180 million years ago.  The Osteoglossomorpha are fishes commonly referred to as bonytongues, because of the teeth on the tongue and roof of the mouth.  Other well-known bonytongues fishes include the Mooneye, Goldeye, Arapaima, Elephantfishes, and the featherback knifefishes.  Today, we need to preserve and protect the remaining populations of the Asian Arowana so that there will be founders to restore wild populations.  Don't be tempted to buy an Asian Arowana.  Let’s ensure that this symbol of good luck and prosperity has a future as long as its past. 

 

References

Austin, C. M. et al. 2015. Whole genome sequencing of the Asian Arowana (Scleropages formosus) provides insights into the evolution of ray-finned fishes. Genome Biology and Evolution 7(10): 2885-95; doi: 10.1093/gbe/evv186

Koh, L.P., D. Sheil, T.M. Lee, X. Giam, L. Gibson, and G.R. Clements. 2013. Biodiversity state and trends in southeast Asia. Chapter 357 in Encyclopedia of Biodiversity, Volume 1.  

Kottelat, M. 2013. Scleropages formosus. The IUCN Red List of Threatened Species 2013: e.T20034A9137739. http://dx.doi.org/10.2305/IUCN.UK.2011-1.RLTS.T20034A9137739.en. Downloaded April 15, 2016