COLLEGE OF AGRICULTURAL, CONSUMER AND ENVIRONMENTAL SCIENCES

Toxic Golden ( parvum)

Revised by Rossana Sallenave1

aces.nmsu.edu/pubs • Cooperative Extension Service • Circular 647

WHAT ARE The College of ? Algae are primitive, mainly Agricultural, aquatic photosynthetic organisms that contain Consumer and chlorophyll and lack true stems, roots, and leaves. Environmental Algal blooms (an explosive increase in the popula- Sciences is an tion of algae) are common in aquatic environments, engine for economic and harmful algal blooms (HABs) can cause substan- tial problems to marine and and community Figure 1. . Photo courtesy freshwater resources. of Texas Parks and Wildlife Department © 2006 Prymnesium parvum, (Greg Southard, TPWD). development in New commonly referred to as “golden alga,” is a microscopic (about 10 µm), flagellated alga that is Mexico, improving capable of producing toxins that can cause extensive fish kills. This algal is found worldwide (Edvardsen and Paasche, 1998) and the lives of New is most often associated with estuarine or marine waters, but it can also occur in inland waters that have a relatively high mineral con- Mexicans through tent. Salinity appears to be the main factor controlling its distribu- tion (Nicholls, 2003). academic, research, The first confirmed blooms ofP. parvum in North America were identified in Texas in 1985 on the Pecos River (James and De La Cruz, and Extension 1989). Since then, fish kills caused by golden algae blooms have oc- curred in 33 reservoirs in Texas along major river systems, including programs. the Brazos, Canadian, Rio Grande, Colorado, and Red Rivers, and have resulted in more than an estimated 34 million fish killed and tens of millions of dollars in lost revenue (Sager et al., 2008; Southard et al., 2010). Prymnesium parvum has invaded reservoirs and river sys- tems in 23 other states, including all southern regions of the USA and more recently some northern states, including Colorado, Wyoming, Nebraska, Iowa, Washington, Pennsylvania, West Virginia, and Maine (Sager et al., 2008; Roelke et al., 2016). In New Mexico, P. parvum was first reported in the 1980s (New Mexico Department of Game and Fish [NMDGF], 2004). From 2002 All About Discovery!TM New Mexico State University 1Extension Aquatic Ecology Specialist, Department of Extension Animal Sciences and Natural aces.nmsu.edu Resources, New Mexico State University. to 2007, P. parvum blooms caused extensive fish ARE GOLDEN ALGAE HARMFUL TO kills in Brantley, Bataan, and Carlsbad Municipal HUMANS OR OTHER ANIMALS? Reservoirs in the lower Pecos River (New Mexico Prymnesium parvum blooms are not considered a Aquatic Management Plan, 2008). public health threat. Unlike , another toxic Blooms were also reported in isolated ponds near alga, toxins that golden algae produce do not ap- Eunice and Roswell (NMDGF, 2004, 2005), and pear to have a negative effect on other wildlife, live- toxic golden algae blooms led to fish kills in McAl- stock, or humans. However, scientists have stressed lister Lake in Las Vegas (S. Hopkins, personal com- that there is currently insufficient scientific evi- munication, January 22, 2009). dence to conclusively state that there are no health risks to terrestrial organisms or humans. As a com- mon sense precaution, dead or dying fish should WHAT DO GOLDEN ALGAE LOOK LIKE? not be consumed. These single-celled organisms are ellipsoid or oval in shape, with cells ranging from 8 to 11 µm in length and 4 to 6 µm in width (Green et al., UNDER WHAT CONDITIONS DO 1982). Each P. parvum cell has two equal “tails” GOLDEN ALGAE BLOOMS OCCUR? called flagella and a short, flexible peg-like organ- Although it can exist in waters without causing elle called a haptonema (Figure 1). The flagella are harm, under certain environmental conditions, P. used for motility and the haptonema may be used parvum can gain a competitive edge over other al- for attachment or feeding. Prymnesium parvum gal species, and algal blooms can be initiated. The cells have two saddle-shaped that are presence of blooms of P. parvum does not necessar- usually yellow-green to olive in color. Microscopic ily mean the algae will produce and secrete prym- examination of subsurface water samples (P. par- nesins into the water, and in fact studies suggest vum is light sensitive and avoids the water surface) that bloom density and toxicity are not strongly at magnifications of 400 to 1,000× is required for correlated (Shilo, 1981). Toxicity appears to be identification, and confirmation requires the -ex enhanced by temperatures lower than 86°F (30°C) amination of the scale morphology using electron (Shilo and Ashner, 1953), by pH greater than 7.0, microscopy or molecular-based techniques (Ga- and when cells are grown under nutrient-limited luzzi et al., 2008). Proper identification of this alga conditions (Dafni et al., 1972; Granéli and Johans- requires experience. son, 2003; Hambright et al., 2014). Studies have shown not only that P. parvum becomes more toxic when nutrients are limited but also that toxicity HOW DO GOLDEN ALGAE KILL FISH? was reduced when nutrients were added to natu- Golden algae are believed to produce a number of ral plankton communities undergoing P. parvum toxins, collectively known as prymnesins, which blooms (Kurten et al., 2007; Roelke et al., 2007; include an ichthyotoxin, or fish toxin (Ulitzer Errera et al., 2008). and Shilo, 1966); a cytotoxin (a substance that is In the south-central USA, golden algae blooms toxic to cells) (Ulitzer and Shilo, 1970); and a he- and associated fish kills almost always occur during molysin (a protein that causes the destruction of the cooler winter and spring months (Hambright et red blood cells) (Ulitzer, 1973). The ichthyotoxin al., 2010; Southard et al., 2010; VanLandeghem et adversely affects gill-breathing organisms such as al., 2014; Hambright et al., 2015). This is the time fish, bivalves, crayfish, gilled amphibians, and also of year when environmental conditions (cooler some species of plankton. The toxin damages the temperatures, limited nutrients) are not favorable permeability of gill cells, which then makes them to other algae, and it appears to give golden algae susceptible to any toxins present in the water, in- an advantage. However, the exact environmental cluding the P. parvum toxin itself (Olli and Trunov, conditions favoring toxic algal blooms are not clear, 2007). The gills lose their ability to exchange water and even though factors such as water temperature and absorb oxygen and bleed internally, resulting in and salinity are somewhat helpful in predicting death of the organism by asphyxiation. future blooms, there are many exceptions that have been reported. For example, if golden algae become

Circular 647 • Page 2 Figure 2. Foam is characteristic of P. parvum blooms. Figure 3. Appearance of gills of a dying largemouth bass Photo courtesy of Texas Parks and Wildlife Department during an . Photo courtesy of Texas Parks and © 2006 (Joan Glass, TPWD). Wildlife Department © 2006 (Greg Southard, TPWD). abundant in the overall algal community, they can human presence or other disturbance. They may try persist all year despite rising temperatures, and fish to leap from the water to avoid the toxins. If clean kills can occur during summer months, as has hap- water flows into the affected body of water, fish will pened in some Texas lakes and rivers. It does appear often accumulate around this freshwater source. that the most important factor influencing the tox- Signs of intoxication include redness or bleeding in icity of P. parvum blooms is the relative amount of the gills, at the base of the fins, around the mouth nitrogen and phosphorus found in the water, with area, and along the belly, and the fish may be cov- toxicity increasing when both of these nutrients are ered with mucous (Figure 3). Young fish are often limited (Johansson and Granéli, 1999; Roelke et more sensitive to the toxins than adults. In the early al., 2007, 2016; Errera et al., 2008; Hambright et stages of intoxication, the effects are reversible if the al., 2014). fish can move to uncontaminated water. Ecologi- cal impacts will vary depending on the length and severity of the toxic bloom. In larger water bodies SIGNS OF GOLDEN ALGAE BLOOMS with access to fresh water, toxic blooms may not kill AND FISH INTOXICATION all the fish present. However, in shallow hatchery ponds, the entire population of fish may be killed if Appearance of the Water the toxic bloom is not treated promptly. When the population of golden algae increases dur- ing a bloom cycle, the water may begin to turn yel- lowish, yellow-copper, or a copper-brown tea color. MANAGING GOLDEN ALGAE Another sign of P. parvum blooms can be foaming at the water surface if agitated or aerated, such as Monitoring for Presence where there is wave action (Figure 2). However, it In New Mexico, the Department of Game and is important to note that these conditions can be Fish (NMDGF) currently monitors bodies of water caused by other sources, and fish kills have been re- for the presence of P. parvum and investigates the ported in waters where these visual conditions were causes of its spread. Water samples are collected and not apparent. examined microscopically to determine if the alga is present. Once the presence of P. parvum is con- Signs of Intoxication firmed, cell counts are conducted to estimate the Fish affected by P. parvum toxins behave erratically. density of algal cells in the water. Recently, a rapid They may swim slowly below the surface, accumu- test for the detection of P. parvum using a specific late in the shallows, or show no normal avoidance of monoclonal antibody and solid-phase cytometry

Circular 647 • Page 3 (the counting of cells) was developed by West et al. as well as large numbers of invertebrate food organ- (2006). In another study, a method using real-time isms such as rotifers and cladocerans (Boyd, 1990). quantitative PCR (a molecular technique used to Excessive additions of nutrients can lead to pH and produce large quantities of DNA) was developed dissolved oxygen problems. In addition to using for the rapid detection and quantification ofP. par- ammonium sulfate and copper sulfate to control P. vum (Galluzi et al., 2008). parvum, Chinese carp breeders have used suspend- ed solids (mud), the addition of fertilizer (manure), Estimating Toxicity of Golden Algae and reduced salinity with varying degrees of success The presence of golden algae does not necessarily (Guo et al., 1996). Ultraviolet light and ozonation mean toxins will be produced. To test for the pres- have been successfully used to control P. parvum in ence of toxins and estimate toxicity, a bioassay (a small volumes of water, but these treatments may test to measure biological activity or potency of a not be feasible for ponds and reservoirs due to the substance) can be used (Ulitzer and Shilo, 1964). cost and required equipment (Sager et al., 2007). This test can identify waters that have high enough Other methods, including ultrasonic vibrations, concentrations of the toxin to pose a risk to fish, barley straw, and probiotics, were investigated by and can help to decide if treatments are warranted. TPWD to determine their effectiveness at con- The bioassay involves exposing test fish to various trolling P. parvum blooms and toxicity, but were dilutions of the water in question amended with deemed ineffective (Grover et al., 2007; Sager et a chemical solution known as a cofactor. This co- al., 2007). factor enhances the potency of the ichthyotoxin, When deciding to apply any algaecide, it is im- which enables the detection of sub-lethal levels of portant to first obtain all regulatory approvals and the toxin. The bioassay currently used by Texas permits. Only those treatments approved by the Parks and Wildlife Department (TPWD) has been U.S. Environmental Protection Agency and the adapted from the Israeli test, and the methods New Mexico Department of Agriculture can be can be found in Appendix B at the following link: used in New Mexico. It is also important to follow http://www.tpwd.state.tx.us/publications/pwdpubs/ all label instructions and restrictions to comply media/pwd_rp_t3200_1138_appendices.pdf. with federal law. While these chemical methods may be successful Treatments in controlling P. parvum blooms in aquaculture fa- Management guidelines and treatments for control- cilities, their use in natural systems is problematic ling golden algae in ponds and small reservoirs are because of regulatory restrictions and the high risk covered in detail by the TPWD (Sager et al., 2007). of negative impacts on non-target species. Further- In aquaculture pond facilities, P. parvum blooms more, while ponds and smaller reservoirs (less than are currently controlled primarily by the addition a few hundred acres) can be successfully treated of chemicals possessing algicidal properties. These with these chemicals, it is simply not financially include ammonium sulfate (Barkoh et al., 2003) or or logistically feasible to apply algaecides to larger copper-based algaecides to reduce population densi- lakes, reservoirs, and rivers. For these reasons, ties, and potassium permanganate to reduce toxicity feasible management techniques are currently not (Dorzab and Barkoh, 2005; Barkoh et al., 2010). available for large bodies of water in New Mexico, Adding nutrients has also been shown to suppress such as the Pecos River, and golden alga is cur- population growth and production of toxins in rently virtually impossible to eradicate from such aquaculture ponds (Kurten et al., 2010). However, natural systems. One possible avenue to pursue for all these approaches have some drawbacks. The long-term control of P. parvum may be to reduce concentrations of ammonium sulfate required to salinity to levels that are below tolerance levels of control P. parvum may produce concentrations of the alga, either by source attenuation or dilution un-ionized ammonia that can be toxic to some fish of the water through manipulations of water lev- (Barkoh et al., 2003, 2004). Copper sulfate is effec- els and flow, or some combination of the two (S. tive in reducing the number of algal cells, but has Hopkins, personal communication, January 22, no effect on their toxicity (Sager et al., 2007) and 2009). Addition of nutrients is a strategy that has may kill desirable algae along with the golden algae, proven to be effective in suppressing growth of

Circular 647 • Page 4 P. parvum during in-lake mesocosm experiments • Never move water, live animals, or plants from one (Roelke et al., 2007; Errera et al., 2008), and body of water to another because you may also large-scale fertilization to help control blooms of transplant undesirable species such as P. parvum. P. parvum has been considered, but that could lead to other ecological problems (S. Denny, personal communication, January 9, 2009). The use of clay WHERE CAN I LEARN MORE minerals to flocculate (form into a lumpy, aggre- ABOUT GOLDEN ALGAE? gated mass) and sediment algal blooms from the The TPWD has a Golden Alga Task Force that water column has shown some promise in labora- works with researchers, other agencies, and inter- tory and field trials (Sengco and Anderson, 2005). ested stakeholders within and outside Texas to bet- The practice involves adding clay slurries directly ter understand, monitor, and control P. parvum. To over an algal bloom, which subsequently form ag- find out more about golden algae, bloom status re- gregates of algal cells and clay that settle out of the ports, and research and management of P. parvum, water column. Algal cell removal efficiency appears visit the TPWD website at www.tpwd.state.tx.us/ to be best when clays and chemical flocculants are landwater/water/environconcerns/hab/ga/. combined (Sengco and Anderson, 2005).

REFERENCES WHAT CAN I DO TO HELP PREVENT Barkoh, A., D.G. Smith, and J.W. Schlechte. THE SPREAD OF GOLDEN ALGAE? 2003. An effective minimum concentration of Dead or dying fish or large numbers of fish behav- un-ionized ammonia nitrogen for controlling ing erratically should be reported to authorities as Prymnesium parvum. North American Journal of quickly as possible. In New Mexico, fish kills are Aquaculture, 65, 220–225. investigated by the New Mexico Environment De- Barkoh, A., D.G. Smith, and G.M. Southard. partment (NMED) in collaboration with NMDGF 2010. Prymnesium parvum control treatments Regional Offices. Contact the Surface Water Qual- for fish hatcheries.Journal of the American Water ity Bureau of NMED at http://www.nmenv.state. Resources Association, 46, 161–169. nm.us/swqb/FishKills, or one of the NMDGF Area Barkoh, A., D.G. Smith, J.W. Schlechte, and J.M. Operations Regional Offices at http://www.wildlife. Paret. 2004. Ammonia tolerance by sunshine state.nm.us/home/contact/location-map/, with as bass fry: Implication for use of ammonia sulfate much information as you can provide (species, size, to control Prymnesium parvum. North American approximate number of fish affected, and location Journal of Aquaculture, 66, 305–311. where fish were observed). Boyd, C.E. 1990. Water quality in ponds for aqua- To prevent the spread of golden algae from one culture. Auburn: Alabama Agricultural Experi- body of water to another, the following precautions ment Station. should be taken. Dafni, Z., S. Ulitzer, and M. Shilo. 1972. Influence • Before leaving a lake or other body of water, of light and phosphate on toxin production and drain all water from the bilge, live wells, and any growth of Prymnesium parvum. Journal of Gen- other water-holding device of your watercraft. eral Microbiology, 70, 199–207. • Rinse out the boat, bilge, live wells, and equip- Dorzab, T., and A. Barkoh. 2005. Toxicity of cop- ment with fresh water and, if possible, allow the per sulfate and potassium permanganate to rain- equipment to dry for two to three days before bow trout and golden alga Prymnesium parvum. using it at another body of water. In A. Barkoh and L.T. Fries (Eds.), Management • For an extra precaution, it is recommended of Prymnesium parvum at Texas state fish hatcher- to spray the surface of equipment with a 10% ies [Management Data Series No. 236, PWD RP bleach solution, allowing a 15-minute contact T3200-1138 (9/05)] (pp. 20–24). Austin: Texas time before rinsing the area with clean water free Parks and Wildlife Department. of algae and allowing it to dry.

Circular 647 • Page 5 Edvardsen, B., and E. Paasche. 1998. Bloom dy- Hambright, K.D., J.D. Easton, R.M. Zamor, J. namics and physiology of Prymnesium and Chrys- Beyer, A.C. Easton, and B. Allison. 2014. Regu- ochromulina. In D.M. Anderson, A.D. Cembella, lation of growth and toxicity of a mixotrophic and G.M. Hallegraeff (Eds.), Physiological ecology microbe: Implications for understanding range of harmful algal blooms (pp. 193–208). Heidel- expansion in Prymnesium parvum. Freshwater berg, Germany: Springer Verlag. Science, 33, 745–754. Errera, R.M., D.L. Roelke, R.L. Kiesling, B.W. Hambright, K.D., J.E. Beyer, J.D. Easton, R.M. Brooks, J.P. Grover, L. Schwierzke, F. Ureña- Zamor, A.C. Easton, and T.C. Hallidayschult. Boeck, J.W. Baker, and J.L. Pinckney. 2008. Ef- 2015. The niche of an invasive marine microbe fect of imbalanced nutrients and immigration on in a subtropical freshwater impoundment. ISME Prymnesium parvum community dominance and Journal, 9, 256–264. toxicity: Results from in-lake microcosm experi- James, T.L., and A. De La Cruz. 1989. Prymnesium ments. Aquatic Microbial Ecology, 52, 33–44. parvum Carter (Chrysophyceae) as a suspect of Galluzzi, L., E. Bertozzini, A. Penna, F. Perini, A. mass mortalities of fish and shellfish communi- Pigalarga, E. Graneli, and M. Magnani. 2008. ties in western Texas. The Texas Journal of Science, Detection and quantification ofPrymnesium par- 41, 429–430. vum (Haptophyceae) by real-time PCR. Letters Johansson, N., and E. Granéli. 1999. Influence in Applied Microbiology, 46, 261–266. of different nutrient conditions on cell density, Granéli, E., and N. Johansson. 2003. Effects of the chemical composition and toxicity of Prymne- toxic Prymnesium parvum on the sium parvum (Haptophyta) in semi-continuous survival and feeding of a ciliate: The influence cultures. Journal of Experimental of different nutrient conditions. Marine Ecology and Ecology, 239, 243–258. Progress Series, 254, 49–56. Kurten, G.L., A. Barkoh, D.C. Begley, and L.T. Green, J.C., D.J. Hibberd, and R.N. Pienaar. 1982. Fries. 2010. Refining nitrogen and phosphorus The of Prymnesium (Prymnesiophy- fertilization strategies for controlling the toxigen- ceae) including a description of a new cosmo- ic alga Prymnesium parvum. Journal of the Ameri- politan species, P. patellifera sp. nov., and further can Water Resources Association, 46, 170–186. observations on P. parvum N. Carter. British Phy- New Mexico Aquatic Invasive Species Advisory cological Journal, 17, 363–382. Council. 2008. New Mexico aquatic invasive spe- Grover, J.P., J.W. Baker, F. Ureña-Boeck, B.W. cies management plan. Brooks, R.M. Errera, D.L. Roelke, and R.L. New Mexico Department of Game and Fish. June Kiesling. 2007. Laboratory tests of ammonium 10, 2004. New Mexico wildlife news. and barley straw extract as agents to suppress New Mexico Department of Game and Fish. Feb- abundance of the harmful alga Prymnesium par- ruary 28, 2005. New Mexico wildlife news. vum and its toxicity to fish.Water Research, 41, Nichols, K.H. 2003. Haptophyte algae. In J.D. 2503–2512. Wehr and R.G. Sheath (Eds.), Freshwater algae Guo, M., P.J. Harrison, and F.J.R. Taylor. 1996. of North America: Ecology and classification (pp. Fish kills related to Prymnesium parvum N. 511–521). San Diego, CA: Academic Press. Carter (Haptophyta) in the People’s Republic of Olli, K., and K. Trunov. 2007. Self-toxicity of China. Journal of Applied Phycology, 8, 111–117. Prymnesium parvum (). Phyco- Hambright, K.D., R.M. Zamor, J.D. Easton, K.L. logia, 46, 109–112. Glenn, E.J. Remmel, and A.C. Easton. 2010. Roelke, D.L., A. Barkoh, B.W. Brooks, J.P. Gro- Temporal and spatial variability of an invasive ver, K.D. Hambright, J.W. LaClaire II, P.D.R. toxigenic in a North American subtropi- Moeller, and R. Patino. 2016. A chronicle of a cal reservoir. Harmful Algae, 9, 568–577. killer alga in the west: Ecology, assessment, and management of Prymnesium parvum blooms. Hy- drobiologia, 764, 29–50.

Circular 647 • Page 6 Roelke, D.L., R.M. Errera, R. Kiesling, B.W. Texas Parks and Wildlife Department. 2003. Brooks, J.P. Grover, L. Schwierzke, F. Ureña- Golden alga (Prymnesium parvum) workshop Boeck, J. Baker, and J.L. Pinckney. 2007. Effects summary report [Online]. Retrieved June 20, of nutrient enrichment on Prymnesium parvum 2009, from https://tpwd.texas.gov/publications/ population dynamics and toxicity: Results from pwdpubs/media/pwd_rp_t3200_1203.pdf field experiments, Lake Possum , USA. Ulitzer, S. 1973. The amphipathic nature of Prym- Aquatic Microbial Ecology, 46, 125–140. nesium parvum hemolysin. Biochimica et Bio- Sager, D., L. Fries, L. Singhurst, and G. Southard physica Acta, 298, 673–679. (Eds.). 2007. Guidelines for golden alga Prym- Ulitzer, S., and M. Shilo. 1964. A sensitive assay nesium parvum management options for ponds system for the determination of the ichthyotox- and small reservoirs (public waters) in Texas. icity of Prymnesium parvum. Journal of General Austin: Texas Parks and Wildlife Department Microbiology, 36, 161–169. (Inland Fisheries). Ulitzer, S., and M. Shilo. 1966. Mode of action of Sager, D.R., A. Barkoh, D.L. Buzan, L.T. Fries, J.A. Prymnesium parvum ichthyotoxin. Journal of Pro- Glass, G.L. Kurten, J.J. Ralph, E.J. Singhurst, tozoology, 13, 332–336. G.M. Southard, and E. Swanson. 2008. Toxic Ulitzer, S., and M. Shilo. 1970. Procedure for Prymnesium parvum: A potential threat to U.S. purification and separation ofPrymnesium par- reservoirs. In M.S. Allen, S. Sammons, and M.J. vum toxins. Biochimica et Biophysica Acta, 201, Macina (Eds.), Balancing fisheries management 350–363. and water uses for impounded river systems (pp. VanLandeghem, M.M., M. Farooqi, G.M. South- 261–273), American Fisheries Society, Sympo- ard, and R. Patiño, 2015. Associations between sium 62, Bethesda, MD. water physicochemistry and Prymnesium parvum Sengco, M.R., and D.M. Anderson. 2005. Removal presence, abundance, and toxicity in west Texas of Prymnesium parvum through clay and chemi- reservoirs. Journal of the American Water Resources cal flocculation [PWD RP T3200-1177]. Austin: Association, 51, 471–486. Texas Parks and Wildlife Department. West, N.J., R. Bacchieri, G. Hansen, C. Tomas, P. Shilo, M. 1981. The toxic principles of Prymnesium Lebaron, and H. Moreau. 2006. Rapid quanti- parvum. In W.W. Carmichael (Ed.), The water fication of the toxic algaPrymnesium parvum in environment: Algal toxins and health, vol. 20 (pp. natural samples by the use of a specific monoclo- 37–47). New York: Plenum Press. nal antibody and solid-phase cytometry. Applied Shilo, M., and M. Aschner. 1953. Factors govern- and Environmental Microbiology, 72, 860–868. ing the toxicity of cultures containing the phyto- flagellatePrymnesium parvum. Journal of General Microbiology, 8, 333–343. Rossana Sallenave is the Extension Southard, G.M., L.T. Fries, and A. Barkoh. 2010. Aquatic Ecology Specialist at New Prymnesium parvum: The Texas experience. Jour- Mexico State University. She earned her nal of the American Water Resources Association, Ph.D. at the University of Guelph in Canada. Her research interests include 46, 14–23. aquatic ecology and ecotoxicology. Her Extension goals are to educate and as- sist New Mexicans on issues relating to watershed stewardship and aquatic eco- system health.

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Revised May 2018 Las Cruces, NM

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