Learning Lessons About Lampreys, by Don Orth

Lampreys are simple fish, but they leave me with many questions. Lampreys and hagfishes are genetically very similar and represent the oldest living groups of vertebrates. These two lineages of mobile Chordates arose well before the appearance of jawed fishes.   Lampreys and hagfish persisted through at least four of five mass extinction events on Earth. How did they survive when most marine organisms perished?    

The appearance of the cranium, eyes, pineal gland, inner ear, olfactory rosettes, lateral line, large brain, and muscular heart, were first evident in the lamprey.  The body form of lampreys is simple and essentially the same as a 360 million year old fossil lamprey described by Gess et al. (2006). Whose blood or flesh did this lamprey feed on?

Lateral views of  (a) a larval lamprey (ammocoete), (b) an adult lamprey, and (c) a hagfish. This figure was originally published in Hardisty et al. (1989). (Royal Society of Edinburgh from Transactions of the Royal Society of Edinburgh: Earth Sciences 80:241–254.

Lampreys have been around a very long time and yet we still don’t know much. The explosion of Sea Lamprey in the upper Great Lakes spurred much research aimed at developing control strategies.  See blog post.   However, there are 22 other species of lampreys in North America in the family Petromyzontidae.  How are they getting along?

The Pacific Lamprey Entosphenus tridentatus has been declining for decades after construction of eight hydroelectric dams on the lower Columbia and Snake Rivers (Close et al. 2002).   Grates that were designed to guide salmon away from the turbine intakes did not protect the weaker-swimming lampreys.  In 2003, conservation groups petitioned the USFWS to list four species of lamprey in Oregon, Washington, Idaho, and California, including the Pacific Lamprey, under the Endangered Species Act.  The petition was deemed unwarranted due to lack of information (Brown et al. 2009).   Eventually 13 stocks were placed on the Endangered Species list and Pacific Lamprey Conservation Initiative emerged.  Will the Pacific Lamprey every recover?

 

The Lost Fish movie trailer.   Full movie available here,

A common genus of lampreys in eastern USA drainages is Ichthyomyzon, which includes 6 species.  Ichthyomyzon are smaller than Sea Lampreys with a single dorsal fin that is continuous with the caudal fin.  The Ohio Lamprey Ichthyomyzon bdellium was described based on a holotype specimen collected from the Ohio River.  Adult Ohio lampreys are parasitic.  Tooth patterns and myomere counts are important traits to identify genera and species.  Are there any hotspots of Ohio Lamprey abundance left?

A major evolutionary change that occurred in the lampreys was the loss of the parasitic life stage.  Paired lamprey species are characterized by larvae that are morphologically and ecologically similar. Only after metamorphosis, can the paired species be reliably identified.   Non-parasitic Mountain Brook Lamprey, Ichthyomyzon greeleyi, likely arose from an ancestor very similar to the Ohio Lamprey; the two paired species are very similar genetically  (McCauley et al. 2015).  The paired species share mitochondrial haplotypes, suggesting a very recent divergence or ongoing gene flow.

Ichthyomyzon is confined to river systems and lakes in central and eastern North America. The distribution patterns the Ichthyomyzon species is still a mystery to all of us.  Isolation and dispersal occur regularly because of the lamprey life cycle.  The larval stage, the ammocoetes live for years in soft sediments in depositional zones found in eddies, backwaters and bends in the river.  Here the ammocetes burrow and filter feed on algae, plankton, and other organic matter.  The blind and toothless ammocoetes of the Ohio Lamprey remain in the substrate for 4 years before metamorphosing into the parasitic form in the mid to late summer.  Here they must depend on water flow through their branchial chamber.  Another key to ammocetes habitat is shade for the photophobic ammocetes.  Diatoms grow and form an incrustration on the interface between the silt and water interface (Dawson et al. 2014).  Larval lampreys are important in nutrient cycling, facilitating the conversion of nutrients derived from detritus and algae into stored biomass. 

Young ammocoetes. Photo by Wester Ross Fisheries Trust. 

Lampreys are ecosystem engineers because the burrowing and feeding activities of larval

lampreys significantly increase substrate oxygen levels (Shirakawa et al. 2013).  The long larval period and burrowing behavior presumably allows the larval lamprey to avoid many predators that would eat these worm-like filter feeders. 

The next stage is the morphological transformation to resemble an adult.  During this phase the eyes and oral sucking disc develop and the sexually immature Ohio Lamprey will then migrate downstream to encounter an abundance of potential host species.  The oral sucking disc of the Ohio Lamprey is designed to lock on to a fish, create a wound, and secrete an anticoagulant so it can feed on blood.   After growing during a parasitic phase of 1 or 2 years, the now sexually mature Ohio Lamprey will migrate upstream to breed and die.  They thereby transfer the sequestered nutrients upstream upon death.  I wonder how populations of the Ohio lamprey persist where there are so many barriers to dispersal between spawning and adult habitats.   

Oral disc of Ohio Lamprey.  Photo by Derek Wheaton.

Spawning behavior has been described for some species. Just watch the video, Lamprey Love, which shows Southern Brook Lamprey in a spawning pit. Ohio Lampreys spawn in late May or early June in shallow pits.  Both males and females use their oral sucking discs to move rocks and create a spawning pit, or redd.   That’s how they got the name stone sucker name, Petromyzon (Petro = stones and myzon= to suckle). Females may also beat fine sediments out of her redd. The female attaches to a rock and the male attaches near the female’s head so they are parallel in the current and released gametes can drift into the nest and attach to the newly prepared rocky bottom.  The nest-building activity of spawning lampreys increases streambed complexity in ways that appear to benefit other fishes and stream invertebrates  (Hogg et al. 2014).

Range of the Ohio Lamprey (NatureServe 2013).

A long period of evolutionary coexistence with large host fishes means that detrimental impact of lamprey on native fish populations is uncommon.   The parasitic adult Ohio Lamprey migrates to larger waters with numerous species of large-bodied fishes.   The occurrence of lamprey scars on these fishes is typically as low as 10%.   Watch this Silver Lamprey locked on an American Paddlefish.   Specialized lamprey predators do not exist.  I wonder about the anti-predator behavior of lamprey.

Channel Catfish dorsal view showing a Chestnut Lamprey scar.  Photo by Michael J. Moore. 

The conservation status of 33 of the 44 species (75 %) has been assessed at a global scale. (Maitland et al. 2014) and at least 12 are at risk.  Jelks et al. (2008) concluded that 43% of North American lamprey species were at some level of risk.  Williams and Williams (2005) concluded that the Ohio Lamprey “declined across its range, probably related to habitat alteration through damming of large rivers and siltation of small streams, which are important reproductive and larval habitats.”  Unfortunately, the population level data on most lamprey species is not adequate for population viability assessment.   Ohio Lamprey is extirpated from many river drainages as it requires excellent water quality and low fine sediment inputs in both upstream and downstream areas of the watershed.  You can view the underwater videos of the Ohio Lamprey spawning after reading a poem on lamprey romance.

Romance for the Jaw Challenged Fishes  (Milton S. Love 2011, p. 6)

What’s the purpose at this season

That I love you without reason

Never felt this way before

As I sweep the river floor

Though your company’s such bliss

Locking lips we just can’t kiss

For mating’s driven by compulsion

Thus we shall triumph, through repulsion.

This poem reminds me that I have so much more to learn about lampreys. Lampreys are not ugly, blood suckers that kill fish. Ancient Romans considered them regal food. They are cultural icons among Native Americans in the Pacific Northwest. In Japan, lampreys were first medicine for night blindness.  Baked lamprey pie is sent to ruling monarchs of England on special occasions.  It is only in the upper Great Lakes where they deserve the invasive title.  Lamprey has become a significant new model for neuroscience investigations of spinal cord regeneration. No one has yet examined all mentions of lampreys in literature. In this Kurt Vonnegut short story lampreys were finding the Great Lakes too vile and noxious even for them. We need to restore and clean up our rivers for lamprey habitat or suffer the “wrath of the lamprey.”

References

Brown, L.R., S.D. Chase, M.G. Mesa, R.J. Beamish, and P.B. Moyle. 2009.  Biology, Management, and Conservation of Lampreys in North America. American Fisheries Society Symposium 72.  Bethesda, Maryland.

Close, D.A., M.S. Fitzpatrick, and H.W. Li. 2002.  The ecological and cultural importance of a species at risk of exinction, Pacific lamprey. Fisheries 27:19-25.

Dawson, H.A., B.R. Quintella, P.R. Almeida, A.J. Treble, and J.C. Jolley. 2014.  The ecology of larval and metamorphosing lampreys.  Pages 75-137 in M.F. Docker, Editor.   Lampreys: Biology, Conservation, and Control. Volume 1.  Fish and Fisheries Series 37. Springer.

Gess, R.W., M.I. Coates, and B.S. Rubidge. 2006. A lamprey from the Devonian period of South Africa. Nature 443:981–984.

Goodman, D.H. and S.B. Reid. 2012. Pacific Lamprey  (Entosphenus tridentatus) Assessment and Template for Conservation Measures in California. U.S. Fish and Wildlife Service, Arcata, California. 117 pp.

Jelks, H.L., and fifteen coauthors. 2011. Conservation status of imperiled North American freshwater and diadromous fishes.  Fisheries 33(8):372-407.

Hogg, R.S., S.M. Coghlan, Jr., J. Zydlewski, and K.S. Simon.  2014.  Anadromous sea lampreys (Petromyzon marinus) are ecosystem engineers in a spawning tributary.  Freshwater Biology 59:1294-1307.

Love, M.S. 2011.  Certainly more than you want to know about the fishes of the Pacific Coast: A postmodern experience.   Really Big Press, Santa Barbara, California.  650 pp.

Maitland, P.S., C.B. Renaud, B.R. Quintella, D.A. Close, and M.F. Docker.  Conservation of Native Lampreys.   2014. Pages 375-428 in M.F. Docker, Editor.   Lampreys: Biology, Conservation, and Control. Volume 1.  Fish and Fisheries Series 37. Springer.

NatureServe. 2013. Ichthyomyzon bdellium. The IUCN Red List of Threatened Species 2013: e.T202616A18234634. http://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T202616A18234634.en. Downloaded on 10 March 2017.

McCauley, D.W., M.F. Docker, S. Whyard, and W. Li.  2015.  Lampreys as diverse model organisms in the genomics era.  BioScience  65:1046-1056.

Shirakawa, O., S. Yanai, and A. Goto. 2013.  Lamprey larvae as ecosystem engineers: Physical and geochemical impact on the streambed by their burrowing behavior. Hydrobiologia 701:313-321.

Williams, M.G., and L.R. Williams.  2005.  Conservation Assessment. Ohio Lamprey Ichthyomyzon bdellium.  U.S. Forest Service, Eastern Region.   26 pp.    Available from: https://www.fs.usda.gov/Internet/FSE_DOCUMENTS/fsm91_054381.pdf

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