Friday, January 20, 2017

Sea Lamprey and Unexpected Costs of Shipping, by Don Orth

Among the many invasive fishes, one of the best-studied invasive fish is the parasitic Sea Lamprey (Petromyzon marinus).  Sea Lamprey is the subject of many vertebrate anatomy labs because they represent a morphologically simple fish.  The Sea Lamprey skeleton is cartilaginous, and they lack jaws, scales, and paired fins.  Sea Lamprey have two closely spaced dorsal fins, functional eyes, and seven gill openings.  The mouth of this blood-sucking parasite is most unique.  Sea Lamprey have a circular oral disc with circular rows of sharp, curved teeth and file-like tongue.  After latching on to a large-bodied fish, the Sea Lamprey uses its teeth to rasp through the skin and feed on the blood. The host may die directly from loss of fluids or indirectly from infections of the wound.  If the host fish survives, it may be attacked again by another feeding Sea Lamprey. The Sea Lamprey is an anadromous species native to the North Atlantic Ocean; they breed in rivers in Europe and North America from Newfoundland to Florida.  Sea Lamprey are in the order, Petromyzontiformes, which encompasses forty known species of lampreys worldwide. However, landlocked populations in the Great Lakes have gotten most attention by scientists and anglers, who have crafted the narrative of invader to control at all costs.
Sea lamprey adult. Photo by Oskar Sindri Gislason
Sea Lamprey were a major, or final, cause of the collapse of major commercial fisheries for Lake Trout Salvelinus namaycush, several Whitefishes Coregonus spp., Burbot Lota lota, and Walleye Sander vitreus in the 1940s and 1950s.  Because the Sea Lamprey reduced populations of these large piscivorous fishes, the next invasive fish to arrive, the Alewife Alosa pseudoharengus, quickly become the dominant prey fish in Lakes Ontario, Huron, and Michigan.  The expansion of the Alewife led to introduction of trout and salmonine fishes in 1968 and creation of new multi-million dollar recreational fisheries.  That management controversy is a subject for another essay (Kitchell and Sass 2008; O’Gorman et al. 2013). 
Sea Lamprey oral disc. Photo by Cory Genovese
Expensive and persistent control efforts to reduce abundance of Sea Lamprey began in Lake Superior and spread eastward so that lamprey control in Lake Ontario began in 1971 and suppression was not evident until 1988.  Current control relies primarily on stream application of two lampricides, 3-trifluoromethyl-4-nitrophenol (don't you love organic chemistry now?), or more simply TFM, and Bayluscide.  TFM and Bayluscide are applied to kill larval Sea Lampreys before they metamorphose and emigrate from spawning streams.  Other control techniques include harvest of adults via trapping, and low-head barriers built to reduce the amount of stream habitats that need to be treated with TFM. For more background, view this video Silent Invaders.   Along with effective Sea Lamprey control efforts, harvest controls, stocking, and restoration have also increased abundance of large-bodied fishes, which are hosts for Sea Lamprey. If they did not have such large economic effects, basic questions on the species would not have been addressed.  Consequently, we know a lot about the Sea Lamprey, certainly more than any other lamprey in the world.
The conventional wisdom always held that the Sea Lampreys first entered the Great Lakes in the 1800s through the man-made locks and shipping canals around Niagara Falls.  Niagara Falls was a natural barrier to Sea Lamprey migration above Lake Ontario.  Completion of Erie Canal provided access to from the Hudson River to Lake Erie. Modification of Welland Canal in 1919 provided access between Lake Ontario and Lake Erie. Consequently, Sea Lamprey first appeared in Lake Erie in 1921, and subsequently were documented in Lake Michigan (1936), Lake Huron (1937), and Lake Superior (1946). But what about the status of Sea Lampreys in Lake Ontario?  Recent DNA analyses supports hypothesis that Sea Lamprey are indigenous to Lake Ontario and introduced in other Great Lakes (Waldman et al. 2004, 2006). Unique alleles found in Lake Ontario, but absent in the Atlantic coast collections, would have taken many thousands of years to develop (Waldman et al. 2009).  It is likely that the populations of Sea Lamprey in Lake Ontario and its tributaries, the Finger Lakes, and Lake Champlain once represented relict populations from the last Pleistocene glaciation.  

Erie Canal (Top) source  and Welland Canal (bottom) source
Because of the emergence of the Sea Lamprey and their economic impacts in the upper Great Lakes, much has been learned about the Sea Lamprey.   How they locate their spawning grounds?  How do they locate mates?   The key is chemical, or pheromone-based communication.    Larvae, or ammocetes, and adult males produce and release unique bile acids.  Adults have a small nasal opening at the top of the head and can detect these bile acids at picomolar concentrations (Li et al. 1995; Li et al. 2002).   These finding led to the hypothesis that the bile acid compounds serve as pheromones.   Controlled behavioral tests supported the hypothesis that the pheromones released by larvae and transported downstream and serve to direct the migration of adults females (Bjerselius et al. 2000; Sorensen and Vreize 2003; Sorensen and Stacy 2004).  This research supports the evolutionary role that pheromones have played as chemical cues to the suitability of spawning and rearing habitat for the Sea Lamprey. This research also paved the way to consider another approach to Sea Lamprey control.  Migratory Sea Lamprey rely heavily on olfactory cues to locate river mouths and direct their upstream movement within rivers (Vrieze et al. 2010).   Pheromones could be used to divert migratory Sea Lamprey to tributaries where they may be trapped, poisoned, or sterilized.  Note the large olfactory bulbs in the lamprey brain image below.  
Sea lamprey brain after R.H. Burne
 Many anadromous fishes use olfactory cues to return to their natal home for spawning. Fish, such as Atlantic Sturgeon, Atlantic Salmon and Striped Bass, show significant differences in haplotype frequencies among rivers.  However, the Sea Lamprey do not return to their natal streams for spawning.  As parasites, the tendency for a regular migration circuit and return to a home river is problematic as their host fishes may disperse the parasite widely.   When adults reach maturity they quit feeding and need to find a suitable river for breeding.    Waldman et al. (2008) collected fin clips from Sea Lamprey from eleven Atlantic Slope rivers.  Examination of haplotype frequencies from mitochondrial DNA confirmed a very low variation among river collection sites. Therefore, the Sea Lamprey regularly inter-breed among rivers and demonstrate a regional panmixia and not homing (Waldman et al. 2008).    

With this knowledge, can we control the invasive Sea Lamprey more effectively?  In theory, yes.   Trapping alone in the absence of lampricides is not sufficient to control Sea Lamprey populations (Holbrook et al. 2016).  However, research is underway now to evaluate strategies to integrate multiple control strategies.   One technique releases large numbers of sterile males in an attempt to thwart successful reproduction.  These sterile males still produce sperm, but that sperm is genetically damaged, thereby reducing the number of viable embryos via lethal mutations.  Sterile release strategies, first tested in the early 1990s in the St Mary’s River, reduced survival of embryos in nests by half (Bravener and Twohey 2016). The graph below supports the significant effect that proportion of sterile males observed on nests had on the mean embryo viability of all nests.
 
Plot of embryo viability and proportion of sterile males on nests (Bravener and Twohey 2016).
The solid line represents the theoretical relationship under a baseline embryo viability of 43.4%. The dashed line represents the line of best fit to the 14 data points.
Another technique uses pheromones to disrupt migrations or attract spawners to areas where sterile males are released and/or where spawning adults may be more effectively trapped.  The pheromone compound can now be synthesized, which makes the technique operational.  The pheromone compound is 7α, 12α, 24-trihydroxy-3-one-5α-cholan-24-sulfate (don’t you love organic chemistry?), or more simply 3k PZS (Li et al. 2012).  Costs to synthesize 3k PZS have decreased substantially in the last ten years (Johnson et al. 2013). Dawson et al. (2016) evaluated strategies for pheromone-baited trapping by calculated expected control and their costs.   The findings support combining lampricides and pheromone-baited trapping technologies at comparable costs.  
 Sea Lamprey wound on Steelhead.    Photo by Boris Kitevski source
While the basic research on the Sea Lamprey has great potential to make control efforts more cost effective, costs will continue into the future.  The current management strategy for some Great Lakes fisheries depends on a strategy of stocking piscivores to drive down populations of the invasive Alewife and Rainbow Smelt and thereby reduce competition and predation effects of these invaders.  This strategy works, however, the net effect is more large-bodied fishes that serve as hosts for the parasitic Sea Lamprey.   Stocking piscivores provides more food for Sea Lamprey and leads to competition among salmon, lake trout, and burbot.  In addition, other invasives, including Zebra Mussel, Quagga mussels, Round Goby, and Tubenose Goby will most certainly complicate the future of Great Lakes fisheries.    There is no simple solution to living with invasive fishes.   In closing, remember that where you stand regarding the Sea Lamprey depends on where you sit.  The Sea Lamprey in its native range do not drive down abundance of large bodied fishes. Rather than a scourge, they play important roles.  In tributaries they are ecosystem engineers, creating patches of deep, rocky, and swift water next to deep, slow, and sandy habitat patches, as well as higher density of benthic invertebrates (Hogg et al. 2014).  

References
Bjerselius, R., and eight coauthors. 2000.  Direct behavioral evidence that unique bile acids released by larval sea lamprey (Petromyzon marinus) function as a migratory pheromone.  Canadian Journal of Fisheries and Aquatic Sciences 57:557-569.
Bravener, G., and M. Twohey. 2016. Evaluation of a sterile-male release technique: A case study of invasive Sea Lamprey control in a tributary of the Laurentian Great Lakes. North American Journal of Fisheries Management 36:1125-1138.
Dawson, H.A., M.L. Jones, B.J. Irwin, N.S. Johnson, M.C. Wagner, and M.D. Szymanski. 2016. Management strategy evaluation of pheromone-baited trapping techniques to improve management of invasive sea lamprey.  Natural Resource Modeling 29:448-469.
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.
Holbrook, C.M., R.A. Bergstedt, J. Barber, G.A. Bravener, M.L. Jones, and C.C. Krueger.  2016.  Evaluating harvest-based control of invasive fish with telemetry: performance of sea lamprey traps in the Great Lakes.  Ecological Applications 26:1595-1609.
Johnson, N.S. M.J. Siefkes, C.M. Wagner, H.A. Dawson, H. Wang, T.B. Steeves, M. Twohey, and W. Li. 2013. A synthesized mating pheromone component increases adult sea lamprey (Petromyzon marinus) trap capture in management scenarios.  Canadian Journal of Fisheries and Aquatic Sciences 70:1101-1108.    
Kitchell, J. F., and G. G. Sass. 2008. Great Lakes ecosystems: Invasions, food web dynamics and the challenge of ecological restoration. Pages 157–170 in D. Waller and T. Rooney, editors. Ecological history of Wisconsin. University of Chicago Press, Chicago, Illinois, USA.
Li., W., P.W. Sorensen, and D.G. Gallaher. 1995. The olfactory system of the migratory sea lamprey (Petromyzon marinus) is specifically and acutely sensitive to unique bile acids released by conspecific larvae. Journal of General Physiology 105:569-587.
Li, W., A.P. Scott., M.J. Siefkes, H. Yan, Q. Liu., S.-S. Yun, and D.A. Gage. 2002.  Bile acid secreted by male sea lamprey that acts as a sex pheromone.  Science 296:138-141. 
Li, K., M.J. Siefkes, C.O.Brant, and W. Li. 2012. Isolation and identification of petromyzestrosterol, a polyhydroxysteroid from sexually mature male sea lamprey (Petromyzon marinus L.). Steroids 77:806-810.
O’Gorman, R., C.P. Madenjian, E.F. Roseman, A.Cook, and O.T. Gorman. 2013. Alewife in the Great Lakes: Old invader – New millennium    Pages 705-732 in W.W. Taylor, A. J. Lynch, and N. J. Leonard editors. Great Lakes Policy and Management: A Binational Perspective, 2nd edition. Michigan State University Press, East Lansing
Sorensen, P.W., and L.A. Vrieze. 2003. The chemical ecology and potential application of the Sea Lamprey migratory pheromone. Journal of Great Lakes Research 29(Supp 1):66-84.
Sorensen, P.W., and N.E. Stacey. 2004.  Brief review of fish pheromones and discussion of their possible uses in the control of non-indigenous teleost fishes.  New Zealand Journal of Marine and Freshwater Research 38:399-417.
Vrieze, L.A., R. Bjerselius, and P.W. Sorensen. 2010.  Importance of the olfactory sense to migratory sea lampreys Petromyzon marinus seeking riverine spawning habitat. Journal of Fish Biology 76:949-964.     
Waldman, J.R., C. Grunwald, N.K. Roy, and I.I. Wirgin. 2004. Mitochondrial DNA analysis indicates sea lampreys are indigenous to Lake Ontario. Transactions of the American Fisheries Society 133:950-960. 
Waldman, J.R., C. Grunwald, and I.I. Wirgin. 2006. Evaluation of the native status of sea lamprey Petromyzon marinus in Lake Champlain based on mitochondrial DNA sequencing analysis. Transactions of the American Fisheries Society 135:1076-1085.
Waldman, J., R. Daniels, M. Hickerson, and I. Wirgin. 2009. Mitochondrial DNA analysis indicates sea lampreys are indigenous to Lake Ontario: response to comment. Transactions of the American Fisheries Society 138: 1190-1197.

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