Source: UNIV OF MINNESOTA submitted to NRP
IDENTIFICATION AND FUNCTIONAL CHARACTERIZATIONS OF SEX PHEROMONES IN CYRINID FISH
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
0138642
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2007
Project End Date
Sep 30, 2013
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIV OF MINNESOTA
(N/A)
ST PAUL,MN 55108
Performing Department
Fisheries & Wildlife
Non Technical Summary
Shallow freshwater ecosystems across the country have become seriously degraded by the common carp, an invasive species of fish introduced from Europe in the late 1800's. This species is extremely abundant because of its high fecundity, low life and physiological resilience, and inflict enormous damage on aquatic ecosystems through its habit of digging into the bottom to acquire food. Presently, the only means available to control the common carp is to poison or drain entire ecosystems, an expensive and unsustainable practice. The purpose of this study is to develop a sustainable integrated pest management scheme for the carp using pheromonal lures to attract carp to traps for removal from threatened ecosystems. Pheromones offer the distinct advantage of being both potent and specific, and easy and inexpensive to apply.
Animal Health Component
(N/A)
Research Effort Categories
Basic
(N/A)
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
1120399107020%
1330399107010%
1350399107010%
3010810102040%
3050810107020%
Goals / Objectives
The overarching goal of this project is to develop a comprehensive understanding of the chemical identities and behavioral functions of pheromones used by common carp so that they can be used in an integrated pest management strategy to control this invasive species. We focus on several pheromones, and their roles, functions, and applications. Pheromones have special promised because 20 years of study of another closely related carp, the goldfish, show that these species rely heavily upon them and that they can be synthesized deployed with relative ease. Five specific objectives are identified: 1. To determine the identity and function of the carp species- specific aggregation pheromone. 2. To determine the identity and function of the male-derived sex pheromone. 3. To determine the identity and function of the ovulatory-female derived sex pheromone. 4. To explore how one or more of these pheromones can be used in an integrated pest management strategy. 5. To determine whether and how the aforementioned pheromones are innately recognized or learned (which would influence how they are deployed).
Project Methods
Juvenile common carp will be raised in the laboratory, some to maturity. Initial studies will explore whether and how juveniles are attracted to each others odors (i.e. aggregation pheromones) in large laboratory mazes. Pilot studies already strongly shown that carp use pheromones and that these mazes are very appropriate way of measuring their presence, now we must identify them. Once pheromonal activity is confirmed studies will attempt to isolate and purify the aggregation pheromone using chemical resins high performance liquid chromatography and a bioassay-guided fractionation scheme which employs olfactory recording and behavior. Chemical analysis using mass spectrometry and nuclear magnetic resonance would follow. If successful, the aggregation pheromone would be synthesized and tested in the field. Simultaneously (and as appropriate) male- and female- derived sex pheromones would be investigated in the same manners. Lastly, laboratory experiments will use instrumental conditioning to determine whether and how the identified pheromones can be learned. The exact procedures pursued will be adjusted in appropriate manners depending upon results and our abilities to find funding sources for each of these objectives.

Progress 10/01/07 to 09/30/13

Outputs
Target Audience: Dr. Sorensen’s primary audience is the scientific community but since the founding of the Minnesota Aquatic Invasive Species Research Center in 2012, his audience has expanded to include management agencies and officials. His scientific audiences include academics working across the globe on invasive biology, chemical ecology, fish physiology and behavior, chemoreception, and aquatic ecology. His management audience includes state departments of natural resources, watershed districts, federal fisheries agencies as well as state legislative bodies (LCCMR, LSOHC, Clean Water Fund). The public at large is also an important audience. Efforts: Dr. Sorensen attended half a dozen national and international and regional scientific conferences in 2013. He and his students and postdocs gave 9 talks at these conferences. He also gave 7 invited talks at local AIS, fisheries, University and environmental groups. Dr. Sorensen reviewed manuscripts for 5 journals as two granting agencies (Sea Grant, NSF). In addition, he now serves on several advisory committees including the Minnesota DNR AIS Advisory Board, Minnesota Asian Carp Task Force, Minnehaha Creek AIS Advisory Board, Mississippi River Basin AIS Panel., and the Midwest Governors Association. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? 14 undergraduate research projects 5 MS degrees 8 postdocs 14 classes 18 contracts and grants for about 17.9 million dollars How have the results been disseminated to communities of interest? Television, radio, local newspapers, books, journal articles, newsletters, web sites, Facebook What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? 1.To determine the identity and function of the carp species-specific aggregation pheromone. It is well established that many fishes, and especially those that live in dark and/or turbid waters (many of which are invasive), recognize each other by their odor and aggregate. The chemical identities of these species-identifying pheromones are unknown although they could be prove useful to attract and remove invasive species. Especially perplexing is the fact that all identified fish sex pheromones, including those of the carps, are relatively common body metabolites. Two explanations appear to exist on how pheromone might be species specific: 1) species-identifying pheromones might be complex yet distinctive mixtures of metabolites, or 2) they might be totally unique product(s). The first step to address which of these possibilities might be the case was to confirm that two important model species, the common carp, Cyprinus carpio, and goldfish, Carassius auratus, release attractive odors that are species-specific and should thus be considered pheromones. Using a two choice maze, Sisler & Sorensen (2007 Behaviour 145:1409) tested groups of six species of fish in two choice mazes and showed that they are uniquely and specifically attracted to their own body odors at low concentrations and that these responses are not influenced by recent experiences. Levesque et al. (2011 Journal of Chemical Ecology 37:219) took the next step using juvenile goldfish and showed that their conspecific odor is indeed discerned by the olfactory sense and that activity may be assigned to mixtures of compounds that includes both the polar and nonpolar chemicals. Intriguingly, the long-standing hypothesis that bile acids are key components of the pheromone was not supported. Following the lead of Levesque et al. (2011), Lim &Sorensen (2011 Journal of Chemical Ecology 37:695) used chemical fractionation of body odors and two-choice mazes to examine the possibility that adult male common carp may also employ distinctive mixtures of unknown body compounds to encode species identity along with mixtures of hormonal products to encode sexual condition, thus answering the question of how common hormonal products (hormonal pheromones) can be species specific. They discovered that while ovulated female goldfish and common carp release slightly different mixtures of F prostaglandins to signal ovulation and sexual receptivity, that species identity was found in unidentified mixtures of bodily metabolites that may be the same as those employed by juveniles, seemingly validating the existence of pheromonal complexes. We have termed such complex multiple component pheromones, ‘pheromone complexes’ and continuing to elucidate their true chemical characteristics. We believe that pheromone complexes are used by many fishes and will be useful in fisheries management. 2. To determine the identity and function of the male-derived sex pheromone. Sorensen and colleagues have also discovered that sexually mature male goldfish and common carp release distinctive male sex pheromones that sexually receptive females discern. Initial work was conducted by Levesque & Sorensen (in preparation for Journal of Experimental Biology) who found that sexually-receptive goldfish are specifically attracted to conspecific males and show no preference for immature conspecifics or heterospecifics. Immunoassay has also shown that these species release large quantities of androstenedione which detect (Sorensen et al. 2005 Journal of Comparative Endocrinology 140:164) and which synergizes the activity polar bodily metabolites to serve as an attractive pheromonal complex. Studies of the common carp (Lim & Sorensen, in preparation for Journal of Chemical Ecology) have shown its males employ both androstenedione and as yet unidentified nonpolar metabolites as a male sex pheromone. 3. To determine the identity and function of he ovulatory-female derived sex pheromone Sorensen has found that male goldfish are attracted to ovulatory goldfish but attempts to identify this pheromone have not progressed. 4. To explore how one if more of these pheromones can be used in an integrated pest management strategy. Lim & Sorensen (2012 journal of Chemical Ecology 38: 127) developed a technique using hormone implants to evoke sex pheromone release in wild, free-ranging carps. Experiment using these fish in Minnesota waters demonstrated that they attract males from a distance of approximately 40 m and thus could be used in integrated pest management, perhaps in the final stages when the last few fishes are being removed. Initial tests of this technique in Lake Sorrel, Tasmania, Australia) were successful and the procedure is being employed in this lake. Ongoing efforts are presently attempting to develop this technique for use in Asian carps (Hypophthalmichthys sp.) in Judas fish in the upper Mississippi River. 5. To determine whether and how these pheromones are innately recognized or learned (which could also influence how they are deployed). A classical conditioning paradigm was developed using pairs of sexually immature goldfish in which fish were rewarded with food 15 seconds they entered a chamber following the addition of specific odorants (conditioned stimulus) after a light was illuminated in the tank. Learning was indicated by increased time spent in the chamber in anticipation of food introduction. Fish were able to rapidly (i.e. within 5 days of training) learn to discern individual L-amino acids (ex. arginine, valine, proline, etc), bile acids (cyprinol sulfate, taurocholic acid sulfate), pheromonal sex steroids (17,20b-dihydroxy-4-pregnen-3-one, 17,20b-dihydroxy-4-pregnen-3-one-20-sulfate, androstenedione) and pheromonal F prostaglandins (prostaglandinF2a and 15keto-prostaglandin F2a). Pheromones took slightly longer to learn but even females (whose olfactory systems are less sensitive to prostaglandins and do not respond behaviorally) responded. Goldfish were also able between odorants, expect for the F prostaglandins (which olfactory recording has suggested may be discerned by overlapping olfactory receptors) and in the case of amino acids, mixtures of these compounds. This is first time that we know of that a vertebrate has been shown to be capable of being trained to respond to identified priming and releasing sex pheromones and demonstrates that these cues could used for conditioning to attract invasive fishes in field settings for removal and control because they are often discerned on species-specific basis. In addition to achieving the aforementioned projected which were described in the initial proposal, Dr. Sorensen’s laboratory conducted a great deal of other work which had notable accomplishments. These are described in a total of 31 peer-reviewed publications. In particular, the investigator has developed what he believes to be the only sustainable non-toxin based invasive fish control program in the world. As part of this project populations of common carp have been controlled through managing populations of predatory sunfish in their nursery areas while their adult are located using radio-tagged Judas fish and removed as needed using targeted winter seining. The investigator has also directed a series of projects on endocrine disrupters which have shown that brief exposure to environmental estrogens may suppress reproductive success in males in natural competitive spawning scenarios but this suppression is not permanent. The work on invasive common carp lead to the establishment of the Minnesota Aquatic Invasive Species Research center. Its ongoing work presently includes work on environmental DNA for monitoring, sexual dimorphism and spawning in Asian carps, sonic deterrents and air curtains and modeling.

Publications

  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Vander Hook, J., P. Tokekar, E. Branson, P.G. Bajer, P.W. Sorensen, and V. Isler. 2012. Local-Search Strategy for Multi-Modal, Multi-Target, Active Localization of Invasive Fish. 13th International Symposium on Experimental Robotics 2012. 1787-1792. Silbernagel, J.J. and P.W. Sorensen. 2013. Direct field and laboratory evidence that a combination of egg and larval predation controls recruitment of common carp in many lakes of the upper Mississippi Basin. Transactions of the American Fisheries Society 142(4): 1134-1140. Stewart, M., Baker, C.L. and P.W. Sorensen 2013. Chemical analysis of aquatic pheromones in fish, Chapter 5 in: Touhara, K. (ed.) Pheromone signaling: Methods and Protocols, to appear in the highly successful series Methods in Molecular Biology, Humana Press. Sorensen, P.W. 2013. Behavioral analysis of aquatic pheromones in fish, Chapter 22 in. Touhara, K. (ed.) Pheromone signaling: Methods and Protocols, Methods in Molecular Biology, vol 1068, 12pages, Humana Press.


Progress 01/01/12 to 12/31/12

Outputs
OUTPUTS: This project had several major outputs in both research and outreach in 2012. Activities were supported by 8 grants and contracts (in addition to the Minnesota Agricultural Experiment Station) which together supported the efforts of a team of a dozen. Three new grant proposals were submitted and funded. The most important of these was a request for funding from the state of Minnesota to establish a collaborative research center to study and develop solutions for local aquatic invasive species (AIS). The Minnesota Aquatic Invasive Species Research Center has now been formed with 3 million dollars in start-up funds and had a successful launch event which received considerable support and press coverage. A lab has been renovated to support these efforts and two postdoctoral fellows and an associate director hired. Another 8.7 million dollars has been requested for continuing Center operations through 2019. Meanwhile, research activities in 2012 focused on: 1) identifying pheromones and feeding cues for carps, and 2) controlling common carp at several field sites using novel but sustainable integrated control strategies. Some time was also spent educating students and faculty at the University as well as colleagues at other institutions and the general public about progress understanding fish pheromones and other integrated control procedures for invasive species. We organized and sponsored two international research symposia (American Fisheries Society and The International Congress on Fish Biology) and delivered approximately two dozen invited talks to international symposia, national groups on AIS, the University and several legislative committees in AIS, and local citizens groups. These efforts were noted in approximately a dozen newspaper (Minneapolis Star Tribune, Pioneer Press, Outdoor News), radio (Minnesota Public Radio) and TV (KARE11, KSTP) accounts. Two courses were taught for both undergraduates and graduate students at the University. Serves on the Mississippi River Basin Panel of the Aquatic Nuisance Species Task Force and an editorial board (Chemical Ecology) while reviewing grants for the University Graduate School (4) and NSF (2). Also is on the Minnesota ad hoc Asian Carp Task Force and the DNR AIS advisory board. PARTICIPANTS: Dr. Peter W. Sorensen is the principal investigator and the only employee who is paid from this project (he is half-time). Dr. Sorensen writes and administers grant proposals/ contracts, manages employees/students, and publishes the data. He also now directs the Minnesota Aquatic Invasive Species Research Center. This past year his team included 3 postdoctoral associates, 2 graduate students, 3 technicians and several undergraduates. Dr. Przemek Bajer headed research on carp ecology and population dynamics. Dr. Ratna Ghosal is directing an analysis of carp sex pheromones. Dr. Eichmiller was recently hired to start working on environmental DNA (eDNA) released by carps. Mr. Brett Miller and Ms. Mary Haedrick served as technicians who assisted Dr. Bajer. Jacob Osborne finished his studies on the distribution of juvenile common carp this year and graduated with a M.S. Justine Koch (MS student) now studies the movement of juvenile carp. Brian Moe, Liz Fox, Danielle Grunzuke, and Reid Swanson worked as undergraduate research assistants. The Sorensen laboratory had many collaborators in 2012. Mr. Daryl Ellison and Jerry Johnston (Minnesota Department of Natural Resources, Fisheries) helped with carp field work. Dr. Vaughan Voller (Civil Engineering University of Minnesota) helped design experimental carp barriers and collaborates on a grant. Dr. Volkan Isler (Computer Science, University of Minnesota) designs robots to track invasive carp and is a collaborator on a NSF grant. Dr. Ed Little with the USGS collaborates with work on Asian carp attractants. Dr. Jon Amberg (USGS) and Dr. Loren Miller (MN DNR) collaborated on a project that measures DNA. Research in 2012 was funded by the Invasive Animals Cooperative Research Centre (Australia), the Legislative-Citizens Commission for Minnesota Resources, The Riley Purgatory Bluff Creek Watershed District, The Ramsey Washington Metro Watershed District, the U.S. Geological Survey, the National Science Foundation (NSF), the Clean Water Fund, and the U.S. Fish &Wildlife Service. TARGET AUDIENCES: Dr. Sorensen's primary audience is the scientific community but with the founding of the Minnesota Aquatic Invasive Species Research Center, his audience has expanded to include management agencies and officials. His scientific audiences include academics working in: invasive biology, chemical ecology, fish physiology and behavior, chemoreception, and aquatic ecology. His management audience includes: state department of natural resources, watershed districts, federal fisheries agencies as well as state legislative bodies (LCCMR, LSOHC, Clean Water Fund). PROJECT MODIFICATIONS: With the formation of the Minnesota Aquatic Invasive Species Research Center and the appointment of Dr. Sorensen as its director. Dr. Sorensen's activities will become somewhat more focused on leadership and administration versus research.

Impacts
The research efforts supported by this project have had several major impacts. First, the laboratory has now demonstrated that a sex pheromone can be used to attract an invasive teleost fish (carp) to areas of lakes where they might be removed - and this finding has been published. The laboratory has also discovered that the abundance of common carp in many Midwestern lakes is naturally controlled by environmental processes via predation pressure by native fish on larval carp and published on this. Ongoing studies in the field and laboratory lend strong credence to this possibility in lakes Susan, Riley, Staring and Phalen and a large scale test is presently underway to manage common carp using integrated pest management practices (IPM). This work is being integrated with invasive plant work with an Aquatic ecology lab and is going well. An experimental bubble curtain system to stop carp movement has been constructed in a local watershed as a proof-of-concept. These are the first experiments to test IPM for teleost fish in the Northern Hemisphere. Several watersheds in Minnesota, Wisconsin, and Iowa are implementing our carp control techniques.

Publications

  • Lim, H.K. and P.W. Sorensen. 2012. Common carp implanted with prostaglandin F2α release a sex pheromone complex that attracts conspecific males in both the laboratory and field. Journal of Chemical Ecology 38: 127-134. (DOI: 10.1007/s10886-012-0062-5)
  • Bajer, P.G., C.J. Chizinski, J.J. Silbernagel, and P.W. Sorensen. 2012. Variation in native micro-predator abundance explains recruitment of a mobile invasive fish, the common carp, in a naturally unstable environment. Biological Invasions 14: 1919-1929. (DOI: 10.1007/s10530-012-0203-3)
  • Bajer, P.G. and P.W. Sorensen. 2012. Estimating the abundance of invasive common carp in small Midwestern lakes using boat electrofishing. North American Journal of Fisheries Management 32: 817-822.


Progress 01/01/11 to 12/31/11

Outputs
OUTPUTS: This project had several major outputs in both research and education/ outreach in 2011. These activities were supported by 5 grants and contracts (in addition to this one) which together supported the efforts of a team of 2 postdoctoral associates, 4 graduate students, 2 technicians, and 4 undergraduate students. Three new grant/contract proposals were also written and submitted. Research focused on pheromone identification in the highly invasive Asian carps. Silver and big head carp have been found to detect a unique set of hormonal products that presumably function as sex pheromones. Additional strides were made towards identifying the species-identifying pheromone in the common carp through behavioral testing, chemical fractionation and amino acid analysis. Research has also focused on developing an understanding of carp population dynamics and then applying this knowledge in integrated management practices. Common carp populations were estimated in 2 new Minnesota lakes using make-recapture techniques while carp movement was ascertained using both radio and acoustic tags in 8 lakes. Adult carp have been removed from two others and recruitment controlled. Experiments discovered that bluegill sunfish can control carp recruitment. These observations are now being applied in the first ever sustainable program to control this invasive species. In addition to collecting data, considerable effort was spent educating both students and faculty at the University as well as colleagues at other institutions and the general public about progress understanding fish pheromones and other integrated control procedures for fish. Dr. Sorensen taught three courses for undergraduates and graduate students at the university. In addition, he organized a research symposium. The Sorensen lab gave 4 invited talks at national and international meetings and approximately two dozen talks were delivered to local fisheries and watershed groups in Minnesota. Dr. Sorensen serves on the Mississippi River Basin Panel of the Aquatic Nuisance Species Task Force. He also is on the Minnesota ad hoc Asian Carp Task Force. These efforts and the data they have produced were covered by a television show, and several newpapers in both Australia and Minnesota. PARTICIPANTS: Dr. Peter W. Sorensen is the principal investigator and the only employee who is paid from this project (he is half-time). Dr. Sorensen writes and administers grant proposals/ contracts, manages employees/students, and publishes the data. This past year his team included 2 postdoctoral associates, 4 graduate students, 2 technicians and several undergraduates. Dr. Przemek Bajer headed research on carp ecology and population dynamics. Dr. Hangkyo Lim managed studies on the carp sex pheromone. Mr. Brett Miller and Ms. Mary Haedrick served as technicians who assisted Drs. Bajer. Jacob Osborne is a M.S. student in Conservation Biology who studies how to attract and the capture juvenile carp. Mr. Justin Silbernagel is a M.S. student in Conservation Biology who is testing whether and how native fishes can control the survivorship of carp eggs and larvae. Justin successfully defended and Jake will in a few weeks. Justine Koch and Tracy Szela both started graduate programs on carp this summer. Eric Sanft, Brian Moe, Liz Fox and Reid Swanson worked as undergraduate research assistants for the aforementioned groups. The Sorensen laboratory had many collaborators in 2011. Mr. Daryl Ellison (Minnesota Department of Natural Resources, Fisheries) helped with carp field work and aging. Dr. Vaughan Voller (Civil Engineering University of Minnesota) helped design experimental carp barriers with the Sorensen laboratory and collaborates on a grant. Dr. Volkan Isler (Computer Science, University of Minnesota) designs robotic devises to track invasive carp. Chris Wiwinswski and his staff (Inland Fisheries, Tasmania, Australia) assists with pheromone testing. Mr David Austin (CH2MHill) assists with water quality analysis. Research in 2011 was funded by the Invasive Animals Cooperative Research Centre (Australia), the Legislative-Citizens Commission for Minnesota Resources, The Riley Purgatory Bluff Creek Watershed District, The Ramsey Washington Metro Watershed District, the U.S. Geological Survey, and the National Science Foundation (NSF). TARGET AUDIENCES: Dr. Sorensen's primary audience is the scientific community. This includes academics working in a variety of disciplines including: chemical ecology (he seeks to understand how pheromones drive fish behavior and physiology), fish biology (he seeks to advance basic understanding of physiological and behavioral function in fishes); chemoreception (he seeks to understand how odorous cues are perceived by fish); invasion biology (he seeks to understand why and how some fishes are invasive), toxicology (he seeks to understand how toxicants disrupt the well-being of aquatic organisms), and aquatic ecology he seeks to understand the effects of fish on aquatic ecosystems). Another important secondary audience is the group of management agencies which use the information his laboratory gathers to manage aquatic systems and the fishes they contain (ex. state departmentd of natural resources, watershed districts, federal fisheries agencies, etc.). PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
The research efforts supported by this project have had several major impacts. First, the Sorensen laboratory has now demonstrated that a sex pheromone can be used to attract an invasive teleost fish (carp) to areas of lakes with where they might be removed - and finding has been accepted for publication. The Sorensen laboratory has also discovered that the abundance of common carp in many Midwestern lakes is naturally controlled by environmental processes via predation pressure by native fish on larval carp. Ongoing studies in the field and laboratory lent strong credence to this possibility and a large scale test is presently underway to manage the highly invasive common carp using integrated pest management practices. This is the first experiment to test IPM for teleost fish in the Northern Hemisphere. We understand that several watersheds in Minnesota, Wisconsin, and Iowa are implementing our techniques.

Publications

  • Garcia-Reyero. N., C.M. Lavelle, B.L. Escalon, D. Martinović, K.J. Kroll, P.W. Sorensen, and N.D. Denslow, N.D. 2011. Behavioral and genomic impacts of a wastewater effluent on the fathead minnow. Aquatic Toxicology 101: 38-48.
  • Lavelle, C.A. and P.W. Sorensen. 2011. Behavioral responses of adult male and female fathead minnows to a model estrogenic effluent and its effects on exposure regime and reproductive success. Aquatic Toxicology 101: 521-528.
  • Burns, A.C., P.W. Sorensen, and T. R. Hoye. 2011. Synthesis and olfactory activity of unnatural, sulfated 5-bile acid derivatives in the sea lamprey (Petromyzon marinus). Steroids 76: 291-296.
  • Levesque, H., D. Scaffidi, C.A. Polkinghorne, and P.W. Sorensen 2011. A multi-component species identifying pheromone in the goldfish. Journal of Chemical Ecology 37(2): 219-227.
  • Vrieze, L.A., R.A. Bergstedt, and P.W. Sorensen. 2011. Olfactory-mediated stream finding behavior of migratory adult sea lamprey (Petromyzon marinus). Canadian Journal of Fisheries and Aquatic Science 68:523-533.
  • Bajer, P.B., C.J. Chizinski, and P.W. Sorensen. 2011. Using the Judas technique to locate and remove wintertime aggregations of invasive common carp. Fisheries Management and Ecology 18: 497-505.
  • Lim, H.K. and P.W. Sorensen. 2011. Polar metabolites synergize the activity of prostaglandin F in a species-specific hormonal sex pheromone released by ovulated common carp. Journal of Chemical Ecology 37: 695-704.
  • Sorensen, P.W., and P.G. Bajer. 2011. The common carp in: Encyclopedia of Invasive introduced Species. Editors in chief D. Simberloff and M. Rejmanek. University of California Press Berkeley, CA, pp 100-104.
  • Sorensen, P.W., and R. Bergstedt. 2011. The sea lamprey in: Encyclopedia of Invasive introduced Species. Editors in chief D. Simberloff and M. Rejmanek. University of California Press Berkeley, CA, pp. 619-623.
  • Stacey, N.E., and P.W. Sorensen. 2011. Fish Pheromones In: Farrell A.P., (ed.) Encyclopedia of Fish Physiology: From Genome to Environment, volume 2, pp. 1553-1562 San Diego: Academic Press.


Progress 01/01/10 to 12/31/10

Outputs
OUTPUTS: This project encompasses four externally-funded projects had several major outputs in both research and education/ outreach in 2010. While research focused on pheromone identification and its application to control of the invasive common carp, other aspects of the project examined means to control carp and related species. Strides were made towards identifying the female sex pheromone of the common carp through behavioral testing, chemical fractionation and mass spectrometry. These assays demonstrated that the carp sex pheromone is comprised of prostaglandin F2a and unknown polar components. A role for L-amino acids was ruled out in the later instance. An implant system for delivering the female sex pheromone was developed and tested in Australia. A project is also now underway to characterize sex pheromone in the invasive Asian carps. Research also focused on developing an understanding of carp population dynamics and then applying this knowledge. A large set of experiments was also conducted to determine whether and how predatory native fish control carp recruitment by consuming their eggs and larvae. It discovered that bluegill sunfish can control carp. Additionally, common carp populations were estimated in two Minnesota lakes using make-recapture techniques while carp movement was ascertained using both radio and acoustic tags in four lakes. Adult carp have been removed from two systems and recruitment controlled making this the first ever sustainable program to control this invasive species. An experimental air-driven barrier to stop carp movement appears to be successful. Several manuscripts and a book are presently in preparation. In addition to collecting data, considerable effort was spent educating both students and faculty at the University as well as colleagues at other institutions and the general public about progress understanding fish pheromones and other integrated control procedures for fish. Dr. Sorensen taught three courses for undergraduates and graduate students at the university. In addition, he organized two research symposia, one of which was on non-game fishes in Minnesota. An invasive fish symposium was sponsored by our group at the Midwest Fish&Wildife Conference. The Sorensen lab gave three invited talks at national and international meetings and approximately two dozen talks were delivered to local fisheries and watershed groups in Minnesota. Dr. Sorensen serves on the Mississippi River Basin Panel of the Aquatic Nuisance Species Task Force. These efforts were covered by two television shows in Australia and two newspapers. Three new grant/contract proposals were written and submitted. PARTICIPANTS: Dr. Peter W. Sorensen is the principal investigator and the only employee who is paid from this project (he is half-time). Dr. Sorensen writes and administers grant proposals/ contracts, manages employees/students, and publishes the data. This past year his team included 2 postdoctoral associates, 2 graduate students, 2 technician and several undergraduates. Dr. Przemek Bajer headed research on carp ecology and population dynamics. Dr. Hangkyo Lim managed studies on the carp sex pheromone. Dr. Chris Chizinski was responsible for developing an understanding of carp movement patterns and carp recruitment patterns in a model watershed. Jon Sevensen designed and tested fish barrier system. Mr. Brett Miller and Ms. Mary Haedrick served as technicians who assisted Drs. Bajer and Chizinski. Dr. Jacob Osborne is a M.S. student in Conservation Biology who studies how to attract and the capture juvenile carp. Mr. Justin Silbernagel is a M.S. student in Conservation Biology who is testing whether and how native fishes can control the survivorship of carp eggs and larvae. Aaron Claus, Adam Pellegrini, Brian Moe are undergraduate research assistants for the aforementioned groups. The Sorensen laboratory had many collaborators in 2010. Dr. Tom Hoye and students (Department of Chemistry, University of Minnesota) assisted with pheromone chemical identification and synthesis. Mr. Daryl Ellison, Tim Cross and Mike McInerny (Minnesota Department of Natural Resources, Fisheries) helped with carp field work and aging. Dr. Vaughan Voller (Civil Engineering, SAFL, University of Minnesota) helped design experimental carp barriers with the Sorensen laboratory and collaborates on a grant. Dr. Volkan Isler (Computer Science, University of Minnesota) designed robotic devises with us to track invasive carp and submitted grant proposal with us. Mr. Paul Brown (Department of Primary Industries Victoria, Australia) helped with fish aging and modeling. John Digby and his staff (Tasmania Fisheries, Australia) presently assists with pheromone testing. Mr David Austin (CH2MHill) assists with water quality analysis. Research in 2010 was funded by the Invasive Animals Cooperative Research Centre (Australia), Minnesota Sea Grant, the Legislative-Citizens Commission for Minnesota Resources, the Minnesota Department of Natural Resources (Ecological Services), the Minnesota Department of Natural Resources (Fisheries), The Riley Purgatory Bluff Creek Watershed District, The Ramsey Washington Metro Watershed District, and the U.S. Geological Survey. TARGET AUDIENCES: Dr. Sorensen's primary audience is the scientific community. This includes academics working in a variety of disciplines including: chemical ecology (he seeks to understand how pheromones drive fish behavior and physiology), fish biology (he seeks to advance basic understanding of physiological and behavioral function in fishes); chemoreception (he seeks to understand how odorous cues are perceived by fish); invasion biology (he seeks to understand why and how some fishes are invasive), toxicology (he seeks to understand how toxicants disrupt the well-being of aquatic organisms), and aquatic ecology he seeks to understand the effects of fish on aquatic ecosystems). Another important secondary audience are the management agencies which use the information his laboratory gathers to mange aquatic systems and the fishes they contain (ex. state department of natural resources, watershed districts, federal fisheries agencies, etc.). PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
The research efforts supported by this project have had several major impacts. First, the Sorensen laboratory has now demonstrated that a sex pheromone can be used to attract an invasive teleost fish (carp) to areas of lakes with where they might be removed. Second, the Sorensen laboratory also discovered (Bajer and Sorensen, 2009) that the abundance of common carp in many Midwestern lakes is naturally controlled by environmental processes (winterkill) that operate via native fish predation pressure on larval carp. Ongoing studies in the field and laboratory lent strong credence to this possibility and a large scale test is presently underway to manage the highly invasive common carp using integrated pest management practices (IPM). This is the first experiment to test IPM for teleost fish in the Northern Hemisphere. Policies on invasive fish management are presently being evaluated and re-written by the DNR because of this work.

Publications

  • Vrieze, L.A., R.K. Bjerselius, and P.W. Sorensen. 2010. The importance of the olfactory sense to migratory sea lampreys seeking riverine spawning habitat. Journal of Fish Biology 76:949-964.
  • Fine, J.M., and P.W. Sorensen. 2010. Production and fate of the sea lamprey migratory pheromone. Fish Physiology and Biochemistry. 36: 1013-1020.
  • Bajer, P.G, H.K.Lim, M. J. Travaline, B.D. Miller, and P.W. Sorensen. 2010 Cognitive aspects of food searching behavior in free-ranging wild common carp. Environmental Biology of Fishes. 88: 295-300.
  • Sorensen, P.W. and T.H. Hoye, 2010. Pheromones in Vertebrates. In Comprehensive Natural Products Chemistry II; Mander, L., Lui, H.-W. (B.), Eds.; Elsevier: Oxford, 2010; [Vol. 4], pp 225-262.


Progress 01/01/09 to 12/31/09

Outputs
OUTPUTS: This project had several major outputs in both research and education/ outreach in 2009. These activities were supported by six grants and contracts which together supported the efforts of a team of 4 postdoctoral associates, 4 graduate students, 1 technician, and 2 undergraduate students. Three new grant proposals were also written and submitted. Research focused on pheromone identification/ application and invasive fish control. Great strides were made towards identifying the female sex pheromone of the common carp (a highly invasive fish) through behavioral testing, chemical fractionation and mass spectrometry. These assays demonstrated that the sex pheromone is comprised of a mosaic of polar bodily metabolites and several F prostaglandins. The F prostaglandins have been tentatively identified and prostaglandin F appears to be the most important component. Field tests in Minnesota lakes have shown that this mixture can be artificially produced at low cost by implanting adult carp with prostaglandin F and are now being duplicated in Australia where the common carp is also highly invasive. Research also focused on developing an understanding of carp population dynamics and then applying this knowledge in integrated management practices. Common carp populations were estimated in 6 Minnesota lakes using netting and make-recapture techniques while carp movement was ascertained using both radio and acoustic tags in 4 lakes. Aging analysis has shown that carp only recruit following winterkill when predatory fish are absent. This observation is now being applied in the first ever sustainable program to control this invasive species. Several manuscripts were published and three others are presently in preparation. In addition to collecting data, considerable effort was spent educating both students and faculty at the University as well as colleagues at other institutions and the general public about progress understanding fish pheromones and other integrated control procedures for fish. The principal investigator taught two courses for undergraduates and graduate students at the university. In addition, he organized two research symposia, one on non-game fishes in Minnesota, the other on common carp across the world. He and his associates gave 4 invited talks at national and international meetings while 18 talks were delivered to local fisheries and watershed groups in Minnesota. He serves on the Mississippi River Basin Panel of the Aquatic nuisance Species Task Force. These efforts and the data they have produced were covered by two television shows and two newspapers. PARTICIPANTS: Dr. Peter W. Sorensen is the principal investigator and the only employee who is paid from this project (he is half-time). Dr. Sorensen writes and administers grant proposals/ contracts, manages employees/students, and publishes the data. This past year his team included 4 postdoctoral associates, 4 graduate students, 1 technician and several undergraduates. Dr. Przemek Bajer headed research on carp ecology and population dynamics. Dr. Haude Levesque has been responsible for determining identifying carp species-identifying pheromone. Dr. Hangkyo Lim managed studies on the carp sex pheromone. Dr. Chris Chizinski was responsible for developing an understanding of carp movement patterns and carp recruitment patterns in a model watershed. Mr. Brett Miller was the technician who assisted Drs. Bajer and Chizinski. Dr. Jacob Osborne is a Ph.D. student in Conservation Biology who studies how to attract and the capture juvenile carp. Mr. Justin Silbernagel is a M.S. student in Conservation Biology who is testing whether and how native fishes can control the survivorship of carp eggs and larvae. Mr. Mario Travaline earned his M.S. during the summer of 2009 for studies of carp trapping technique while Ms. Candice Lavelle earned her M.S. for discovering how cyprinid minnows respond to endocrine disrupters. Aaron Claus, Adam Pellegrini, Brandon Demuth, and Chris Johnston offered part-time research support as undergraduates to the above groups. The Sorensen laboratory had many collaborators in 2009. Dr. Tom Hoye and students (Department of Chemistry, University of Minnesota) assisted with pheromone chemical identification and synthesis. Mr. Tim Cross and Mike McInerny (Minnesota Department of Natural Resources, Fisheries) helped with carp field work and aging. Dr. Simone Rochfort (Department of Primary Industries Victoria, Australia) assisted with analyzing polar component of carp pheromones. Dr. Vaughan Voller (Civil Engineering, SAFL, University of Minnesota) helped design experimental carp barriers with the Sorensen laboratory and collaborates on a grant. Dr. Volkan Isler (Computer Science, University of Minnesota) designed robotic devises with us to track invasive carp and submitted grant proposal with us. Mr. Paul Brown (Department of Primary Industries Victoria, Australia) helped with fish aging and modeling. John Digby and his staff (Tasmania Fisheries, Australia) presently assists with pheromone testing. Research in 2009 was funded by the Invasive Animals Cooperative Research Centre (Australia), Minnesota Sea Grant, the Legislative-Citizens Commission for Minnesota Resources, the Minnesota Department of Natural Resources (Ecological Services), the Minnesota Department of Natural Resources (Fisheries), The Riley Purgatory Bluff Creek Watershed District, and The Ramsey Washington Metro Watershed District. TARGET AUDIENCES: Dr. Sorensen's primary audience is the scientific community. This includes academics working in a variety of disciplines including: chemical ecology (he seeks to understand how pheromones drive fish behavior and physiology), fish biology (he seeks to advance basic understanding of physiological and behavioral function in fishes); chemoreception (he seeks to understand how odorous cues are perceived by fish); invasion biology (he seeks to understand why and how some fishes are invasive), toxicology (he seeks to understand how toxicants disrupt the well-being of aquatic organisms), and aquatic ecology he seeks to understand the effects of fish on aquatic ecosystems). Another important secondary audience are the management agencies which use the information his laboratory gathers to mange aquatic systems and the fishes they contain (ex. state department of natural resources, watershed districts, federal fisheries agencies, etc.). PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
The research efforts supported by this project have had several major impacts. First, the laboratory has now demonstrated that a sex pheromone can be used to attract an invasive teleost fish (carp) to areas of lakes with where they might be removed. This cue has been largely identified and is being tested and commercialized in Australia. Second, he was awarded a patent for the application and use of a sea lamprey migratory pheromone (US patent # 7,557,097 B2) which is now being tested in the Great Lakes. Third, by correlating water quality and habitat quality with the historical abundance of the carp in restored wetland, the laboratory prove clearly demonstrated the damage caused by common carp and established removal targets. The laboratory also discovered that the abundance of common carp in many Midwestern lakes is naturally controlled by environmental processes (winterkill) that appear to operate via predation pressure on larval carp. Ongoing studies in the field and laboratory lent strong credence to this possibility and a large scale test is presently underway to manage the highly invasive common carp using integrated pest management practices. This is the first experiment to test IPM for teleost fish in the Northern Hemisphere. Another new project is describing with carp movement patterns so they can be controlled while a new project was funded to commence development of novel environmentally-safe barriers to block movement. A Ph.D. project is developing way to attract and trap juvenile common carp using pheromones and bait attractants combined with flows.

Publications

  • Robinson, T.C. Sorensen, P.W., Bayer, J.M. and Seelye, J.G. (2009)Olfactory sensitivity of Pacific lampreys to a lamprey bile acid. Transactions of the American Fisheries Society 138: 144-152.
  • Sorensen, P.W. (2009) Stream water creates a discernable odor gradient that migratory, juvenile American eels may follow inshore. In: Haro, A. J., K. L. Smith, R. A. Rulifson, C. M. Moffitt, R. J. Klauda, M. J. Dadswell, R. A. Cunjak, J. E. Cooper, K. L. Beal, and T. S. Avery, editors. 2009. Challenges for Diadromous Fishes in a Dynamic Global Environment. American Fisheries Society, Symposium 69, Bethesda, Maryland. pp 841-844.
  • Bajer, P.G, Sorensen, P.W. (2009)The superabundance of common carp in interconnected lakes in Midwestern North America can be attributed to the propensity of adults to reproduce in outlying habitats that experience winter hypoxia. Biologcial Invasions. DOI. 10.1007/s10530-009-9528-y
  • Bajer, P.G, Sullivan, G.S., Sorensen, P.W. (2009) Effects of a rapidly increasing population of common carp on vegetative cover and waterfowl in a recently restored Midwestern shallow lake. Hydrobiologia 632: 235-245.
  • Pellegrini, A.F.A., Wisenden, B.D. and Sorensen, P.W. (2009)Bold minnows consistently approach danger in the field and lab in response to either chemical or visual indications of risk. Behavioral Ecology and Sociobiology DOI 10.1007/s00265-009-0854-y


Progress 01/01/08 to 12/31/08

Outputs
OUTPUTS: My activities in 2008 fell into the categories of both research and education. I advised, mentored and arranged funding for three postdoctoral associates, two graduate students and five undergraduate students. Research conducted by this team fell into several categories. Both behavioral and biochemical experiments were conducted to determine the identities and function of male and female sex pheromones in the common carp (an invasive species) as well as the nature of species-identifying pheromone in this species. Particularly good progress was made addressing potency, specificity, and chemical composition. Together with a colleague in chemistry we also synthesized and tested several pheromonal analogues in the sea lamprey, another damaging invasive species for which pheromones are now being employed based on our earlier studies. Other work focused on developing novel bait attractants to train common carp to come to particular areas of lakes so that they can be removed using traps which we also have been designing. In the field, a large experimental carp program was initiated in six lakes to determine when, where and how carp move and what determines their reproductive success. In particular, several thousand fish have been captured and over 100 were radio-tagged and tracked to determine their precise movement patterns. Another group of several hundred carp was sacrificed and aged. Finally, a study on endocrine disruption has been investing whether, how and why wild fish might enter sewage plumes containing environmental estrogens and what the long-term effects of such exposure are. Considerable effort was also spent educating both students and faculty at the University as well as colleagues at other institutions and the general public. I taught three courses for undergraduates and graduate students at the university. In addition, I gave two invited lectures at international scientific meetings on fish pheromones in 2008, three lectures at national-regional meetings, and 5 public lectures to watershed districts and the Minnesota DNR on results of our studies on invasive fishes and their pheromones. My students and postdoctoral associates gave another six talks. Three grants proposals were written and submitted (all were funded) as well as 6 journal articles and 3 book chapters. I published 6 peer-reviewed scientific articles and assisted on 3 university committees and two for scientific organizations. Finally, I spent some time reviewing nearly a dozen journal submissions. PARTICIPANTS: Dr. Peter W. Sorensen is the principal investigator (P.I.) and the only employee paid more that one month a year on this project (he is half-time). As P.I., Dr. Sorensen writes and administers grant proposals that further the fundamental aims of the project, manages employees and students associated with projects that he obtains funding for, writes progress reports and manuscripts, and educates the scientific community and public about progress. Employees and students of Dr. Sorensen who work on projects affiliated with this one include: Dr. Przemek Bajer (research associate responsible for identifying weakness in carp ecology that can be exploited); Dr. Haude Levesque (research associate responsible for indentifying carp aggregation pheromones); Dr. Hangkyo Lim (research associate responsible for identifying carp sex pheromones); Ms. Candice Lavelle (graduate student responsible for answering if endocrine disrupters effect minnows at the population level), Mr. Mario Travaline (graduate student responsible for answering if food odor can be sued to attract carp); Mr. Jacob Osborne (Ph.D. student working on juvenile carp biology and attraction); Mr. Brett Miller (undergraduate part-time help on carp); Mr. Keith Philippe (undergraduate part-time help), Dr. Adam Smith (undergraduate part-time help); and Mr. Aaron Claus (undergraduate part-time help) . We have many collaborators including: Mr. Tim Cross (Minnesota Department of Natural Resources, Fisheries; who helps with carp field work); Mr. Mike Mcinerny (Minnesota Department of Natural Resources [Fisheries] who helps with carp field work); Dr. Tom Hoye and students (Department of Chemistry [University of Minnesota] who help with pheromone chemical identification); Dr. Simone Rochfort and her graduate student, Mr. Aaron Elkins (Department of Primary Industries Victoria [Australia] who analyses carp chemical attractants), and Mr. Paul Brown (Department of Primary Industries Victoria, [Australia] who help with fish aging). Research presently funded in association with this project is funded by the Invasive Animals Cooperative Research Centre (Australia), the Legislative-Citizens Commission for Minnesota Resources, the Minnesota Department of Natural Resources (Ecological Services), the Minnesota Department of Natural Resources (Fisheries), and the Wetlands Initiative (Chicago). TARGET AUDIENCES: My primary audience is the scientific community. This includes academics and professionals working in a variety of disciplines including: chemical ecology (we seek to advance an understanding of how natural chemicals [pheromones in particular] drive animals ecology and behavior); fish biology (we seek to advance basic understanding of physiological and behavioral function in fishes); chemoreception (we seek to understand how odorous cues are perceived by animals [fish]); animal behavior (we seek to understand basic tenants of animal behavior); comparative physiology (we seek to understand how physiological mechanisms drive behavior in fishes); toxicology (we seek to understand how toxicants disrupt the well-being of aquatic organisms); and aquatic ecology (we seek to understand the effects of fish on aquatic ecosystems). An important secondary audience is comprised of the applied ecologists and managers who use this information to mange aquatic systems and invasive fishes; i.e. the biologists and managers in state departments of natural resources, local watershed districts and other governmental agencies that face the problems of remediating the effects caused by invasive fishes. A third target audience are government pollution control agencies (ex. Minnesota Pollution Control Agency, Environmental Protection Agency) which are concerned about nutrient release caused by invasive fish and endocrine disrupters. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
My research has had major outcomes that have increased our understanding of the natural world in ways that will improve quality of life. Research on carp pheromones has now clearly revealed that this species employs pheromonal mosaics - complex mixtures that perceived as single entities. These cues can be diluted close to 100-fold and still attract only this target species. Fractionation using HPLC has demonstrated that pheromone mosaic is comprised of multiple components which in the case of the female sex pheromone include prostaglandin F. Mass spectrometry has confirmed the later conclusion. The carp pheromone systems may be the most fully characterized sex pheromone amongst the vertebrates. Studies using food odors in the laboratory and field have demonstrated that common carp have long memories and can be classically conditioned to enter traps at certain positions of the lakes. Our work ion carp traps demonstrate that design is critical and the classical DNR traps have mouths which are too narrow to be effective. Aging studies of wild carp demonstrate that they live to be over 50 years old but only survive past a year during years when their lakes experience winter hypoxia. Thus, recruitment is rare. Meanwhile studies of predatory fish abundance in study lakes strongly suggest that it is the abundance of these fish (which are especially sensitive to winter hypoxia) which drive survivorship of invasive carp. This is very important discovery because it suggests means exists to control this, the world's most damaging invasive fish species. This progress has stimulated new applied research and public interest and I have given half-a dozen lectures a year on the topic. Three major grants have been funded.

Publications

  • Martinović, D, Denny, J.S., Ankley, G.T., Schmieder, P.K. and P.W. Sorensen. 2008. Temporal variation in the estrogenicity of a sewage treatment plant effluent and its biological significance. Environmental Science and Technology. 42 (9): 3421-3427
  • Barata, E.N., Fine, J.M., Hubbard, P.C., Almeida, O.G., Frade, P., and Sorensen, P.W., Canario, A.V.M. 2008. A sterol-like odorant in the urine of Mozambique tilapia males likely signals social dominance to females. Journal of Chemical Ecology 34(4): 438-449.
  • Fine, J.M. and Sorensen, P.W. 2008. Isolation and biological activity of the multi-component sea lamprey migratory pheromone and new information in its potency. Journal of Chemical Ecology. Journal of Chemical Ecology 34(10): 1259-1267
  • Triballeau N., Van Name, E., Laslier, G., Cai, D., Paillard, G, Sorensen, P.W., Hoffmann, R., Bertrand, H.-O., Ngai, J. and Acher, F.C. 2008. High-potency olfactory receptor agonists discovered by virtual high-throughput screening: molecular probes for receptor structure and olfactory function. Neuron 60: 1-6.
  • Stacey, N.E. and Sorensen, P.W. 2008. Hormonally derived sex pheromones in fish. Chapter 6 in: Fish Reproduction, (eds. Roche, M.J., Arukwe, A., Kapoor, B.G.), Science Publishers, Enfield, N.H., 201-244.
  • Derby, C.D. and Sorensen, P.W. 2008. Neural processing, perception and behavioral responses to natural chemical stimuli by fish and crustaceans. Journal of Chemical Ecology 34(7): 898-914.
  • Sisler, S.P. and Sorensen, P.W. 2008. Common carp and goldfish discern conspecific identity using chemical cues. Behaviour. 145: 1409-1429.


Progress 01/01/07 to 12/31/07

Outputs
OUTPUTS: My work associated with this project had several major outputs that reached people. In addition to my role teaching two courses, writing research papers and grant proposals, I advised and mentored three postdoctoral associates, three graduate students and five undergraduate students in 2007. This group of individuals has conducted a variety of key experiments on pheromonal attraction in the common carp and sea lamprey, the ecology and population dynamics of wild carp, and endocrine disruption caused by effluent from the St. Paul wastewater plant- all of which have produced important results (see Outcomes). Additionally, I served on the program committee for the Association for Chemoreception Sciences for whom I organized a large national meeting. Locally, I organized a symposium on fish biology for the Minnesota Chapter of the American Fisheries Society. I was on the national panel that reviewed the productivity of the Upper Midwest Environmental Sciences Center (a USGS laboratory in LaCrosse, Wisconsin). For public outreach, I gave 4 public lectures to local environmental and watershed organizations and provided advice on invasive fish and water quality to several others. One talk was attended by over 200 citizens (Riley Purgatory Bluff Creek Watershed District). We are now advising these groups on how to remove carp to improve water quality. My students and I attended 25 scientific conferences and workshops, making approximately 28 presentations. I submitted 7 manuscripts to professional peer-reviewed journals and reviewed nine manuscripts. This effort stimulated several invitations to give talks and write reviews. I testified to the Minnesota state legislature twice on environmental issues (invasive fish, endocrine disruption) and to the National Aquatic Nuisance Species Task Force in Washington D.C. (invasive carp). I wrote and submitted three research proposals requesting new funding while writing seven progress reports on projects in progress. Our research has resulted in several specific products. A patent has been filed by the University of Minnesota and is now pending that uses a migratory pheromone we discovered and identified to control invasive sea lamprey. Efforts are now underway to use this technology to control sea lamprey in the Great Lakes. A law was passed by the state legislature after my testimony and editorial assistance that requires the Minnesota Pollution Control Administration to address the threats posed by endocrine disruption. Finally, I published 6 peer-reviewed scientific articles (see Publications below) and many abstracts (not listed). PARTICIPANTS: Dr. Peter W. Sorensen is the principal investigator (P.I.) and only employee paid more that one month a year on this project (he is half-time). As P.I., Dr. Sorensen writes and administers grant proposals that further the fundamental aims of the project, manages employees and students associated with projects that he obtains funding for, writes progress reports and manuscripts, and educates the scientific community and public about progress. Employees and students of Dr. Sorensen who work on projects affiliated with this one include: Dr. Przemek Bajer (research associate responsible for identifying weakness in carp ecology that can be exploited); Dr. Haude Levesque (research associate responsible for indentifying carp aggregation pheromones); Dr. Hangkyo Lim (research associate responsible for identifying carp sex pheromones); Ms. Candice Lavelle (graduate student responsible for answering if endocrine disrupters effect minnows at the population level), Mr. Mario Travaline (graduate student responsible for answering if food odor can be sued to attract carp); Mr. Lance Vrieze (Ph.D. student responsible for determining how sea lamprey locate pheromones and how they might be employed); Mr. Brett Miller (undergraduate part-time help on carp); Mr. Jon Hess (undergraduate part-time help), Mr. Keith Philippe (undergraduate part-time help). We have many collaborators including: Mr. Tim Cross (Minnesota Department of Natural Resources, Fisheries; who helps with carp field work); Mr. Mike Mcinerny (Minnesota Department of Natural Resources [Fisheries] who helps with carp field work); Dr. Tom Hoye and students (Department of Chemistry [University of Minnesota] who help with pheromone chemical identification); Dr. Simone Rochfort and her graduate student, Mr. Aaron Elkins (Department of Primary Industries Victoria [Australia] who analyses carp chemical attractants), and Mr. Paul Brown (Department of Primary Industries Victoria, [Australia] who help with fish aging). Research presently funded in association with this project is funded by the Invasive Animals Cooperative Research Centre (Australia), the Legislative-Citizens Commission for Minnesota Resources, the Minnesota Department of Natural Resources (Ecological Services), the Minnesota Department of Natural Resources (Fisheries), and the Wetlands Initiative (Chicago). TARGET AUDIENCES: My primary audience is the scientific community. This includes academics and professionals working in a variety of disciplines including: chemical ecology (we seek to advance an understanding of how natural chemicals [pheromones in particular] drive animals ecology and behavior); fish biology (we seek to advance basic understanding of physiological and behavioral function in fishes); chemoreception (we seek to understand how odorous cues are perceived by animals [fish]); animal behavior (we seek to understand basic tenants of animal behavior); comparative physiology (we seek to understand how physiological mechanisms drive behavior in fishes); toxicology (we seek to understand how toxicants disrupt the well-being of aquatic organisms); and aquatic ecology (we seek to understand the effects of fish on aquatic ecosystems). An important secondary audience is comprised of the applied ecologists and managers who use this information to mange aquatic systems and invasive fishes ; i.e. the biologists and managers in state departments of natural resources, local watershed districts and other governmental agencies that face the problems of remediating the effects caused by invasive fishes. A third target audience are government pollution control agencies (ex. Minnesota Pollution Control Agency, Environmental Protection Agency) which are concerned about nutrient release caused by invasive fish and endocrine disrupters.

Impacts
My work has had several major outcomes that have significantly increased our knowledge of the natural world in ways that will improve quality of life. We have discovered the common carp, an extremely damaging invasive fish previously thought to be controllable, can be controlled. Indeed, this species commonly experiences recruitment failure (its young fail to survive to adulthood) after severe winters, suggesting that carnivorous (game) fish might be used to control this species. We have also found that the carp can be trained to swim to specific regions of the lake using chemical attractants where they might be netted en masse. There is now clear evidence that the species uses species-specific pheromones that can be isolated and concentrated. All of this progress is stimulated new applied research and public interest and support. For example, my public speaking was rewarded by our research being featured in the Minneapolis Star Tribune, Frontiers of Ecology, Chanhassen Villager, and Northern Wilds magazine. The newspaper story was also distributed by the Associated Press and distributed nationally to at least several dozen outlets. Public awareness of invasive species issues has clearly been raised in a positive manner, especially because we are providing possible solutions. Similar outcomes have occurred at the institutional level. In particular, the Mississippi River Basin chapter of the Aquatic Nuisance Species Task Force is instituting policy changes as a result of a talk I gave in Washington D.C. I was an invited speaker at the University of Queensland (Australia), the University of Canberra (Australia), the University of Algarve (Portugal), and the University of St. Thomas (Minnesota) where I spoke about research progress on fish pheromones and invasive fish control. Concurrently, I have been invited to write two new book chapters and a research review in a peer-review journal, accelerating the fields of chemical ecology, pheromones, and fish biology. One of my new research grant proposals was funded (Wetlands Initiative, Chicago $8,365) and I expect the two others will be in 2008 (Legislative-Citizens Commission for Minnesota Resources, $450,000; Riley Purgatory Bluff Creek Watershed District, $1,070,000). The field of invasive fish control has been greatly enhanced by our efforts and will be for years to come.

Publications

  • Martinovic, D., Hogarth, W.T., Jones, R.E., and Sorensen, P.W. 2007. Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows. Environmental Toxicology and Chemistry. 26(2): 271-278.
  • Hoye, T.E., Dvornikovs, V., Fine, J.M., Anderson, K.R., Jeffrey, C.S., Muddiman, D.C., Shao, F., Sorensen, P.W., and J. Wang. 2007. Details of the structure determination of the sulfated steroids PSDS and PADS: new components of the sea lamprey (Petromyzon marinus) migratory pheromone. Journal of Organic Chemistry. 72: 7544-7550.
  • Martinovic, D, Denny, J.S., Ankley, G.T., Schmieder, P.K. and P.W. Sorensen. 2007. Temporal variation in the estrogenicity of a sewage treatment plant effluent and its biological significance. Environmental Science and Technology. October 12, 2007 web release date.
  • Appelt, CA, and Sorensen, P.W. 2007. Female goldfish signal spawning readiness by altering when and where they release a urinary pheromone. Animals Behaviour 74: 1329-1338.
  • Sorensen, P.W. and Hoye, T.E. 2007. A critical review of the discovery and application of a migratory pheromone in an invasive fish, the sea lamprey, Petromyzon marinus L. Journal of Fish Biology 71 (supplement D): 100-114.
  • Hobson, K.A., Smith, R.J.F, and Sorensen, P.W. 2007. Applications of stable isotope analysis to tracing nutrient sources of Hawaiian gobioid fishes and other stream organisms. In: Evenhuis, N.L. & Fitzsimons, J.M. (eds.), Biology of Hawaiian Streams and Estuaries. Bishop Museum Bulletin in Cultural and Environmental Studies 3, 99-112, Honolulu, Hawaii.
  • Stacey, N.E. and Sorensen, P.W. 2007. Hormonally derived sex pheromones in fish. Chapter 6 in: Fish Reproduction, (ed. K. Pandy), Oxford Press, New Delhi, 201-243.


Progress 01/01/06 to 12/31/06

Outputs
The overarching goal of my research program is to develop an understanding of the role that aquatic chemicals play in lives of fishes so that this understanding may be used to benefit fisheries. I have two specific objectives and am using funds from the Agriculture Experiment Station to fund that part of my salary dedicated to managing these activities. My first objective is to determine the identity and function of pheromones (potent chemical signals that pass between organisms of the same species) so that they may ultimately be employed to control nuisance/ invasive species of fish for which very few options presently exist. The second is to determine whether and how endocrine disrupters (chemicals released to the environment that mimic the actions of hormones) influence the reproductive health of fishes. The link between these objectives is that many fish sex pheromones are derived from hormones. During the past year I have several projects devoted to both objectives which derive considerable supplemental funding from various agencies including the Great Lakes Fishery Commission (GLFC), Minnesota Sea Grant; Legislative-Citizen Commission on Minnesota Resources, Invasive Animal Cooperative Research Centre, and the Minnesota Department of Natural Resources. Significant progress has been made on all of projects this year. The sea lamprey migratory pheromone has now been isolated, structurally elucidated, synthesized and found to be comprised of 3 unique disulfated steroids. In collaboration with others, we have also now shown this pheromone will attract migratory sea lamprey in the field at very low concentrations. It is presently being developed as a new control strategy and three patent applications have been filed and negotiations are underway between the University and GLFC about developing this new strategy further. My lab has also discovered that the common carp releases a species-specific aggregation pheromone that has potential for use in its control. The cue is released by male, female, and immature carp and it has been isolated. New experiments will identify it. Simultaneously, field work is underway to determine whether and how common carp might be controlled using pheromones and other removal schemes. Interestingly, we are finding compelling evidence of recruitment failure in Minnesota lakes suggesting, there is hope that integrated pest management strategies could be successfully developed for this species. A statistical model to help control this species is also now being developed. Funds have been awarded by the Australian government (IA-CRC) to develop sex pheromones for use in carp control. As part of my second objective, my laboratory has discovered that endocrine disrupting compounds (EDCs) with estrogenic actions are found in waters discharged by the Duluth (MN) sewage treatment plant and which reduce the competitive reproductive success of male minnows. Very recently, we found that these effects are sex specific, at least in the effluent released by the Twin Cities sewage treatment plant. Experiments are underway to explain why and how EDCs have these actions any might be remediated.

Impacts
Likely the greatest threat to the fisheries and waterfowl living in the lakes, large rivers, and wetlands of the Upper Midwest are nonindigenous, invasive species, for which no control strategies other than whole-ecosystem poisoning exist. We are making excellent progress towards developing pheromones as a new tool in their management. Ours will be the first international patent to use pheromones to control a vertebrate. The common carp is the most damaging species in inland waters and many millions are spent attempting (with little success) to control it. We seek to bring new/ modern science, technology, and thinking to this process. Similarly, although it clear that pollutants that disrupt hormonal function of fish and wildlife are released by many sewage treatment plants, the precise nature of this threat is as yet obscure. We are finding that the threat is very real but very likely primarily to gene-flow within populations, a finding with insidious ramifications.

Publications

  • Wagner, C.M., Jones, M.L., Twohey, M.B., and P.W. Sorensen 2006. A field test verifies the pheromones can be useful for sea lamprey (Petromyzon marinus) control in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 63: 475-479.
  • Baker, C. F, Carton, A.G., Fine, J.M., and Sorensen, P.W. 2006. Can bile acids function as migratory pheromones in banded kokopu Galaxius fasciatus (Gray)? Ecology of Freshwater Fishes 15: 275-283.
  • Fine, J.M., Sisler, S.P., Vrieze, L.A., Swink, W.D. and Sorensen, P.W. 2006. A practical method for obtaining useful quantities of pheromones from sea lamprey and other fishes for identification and control. Journal of Great Lakes Research 23(4): 832-838.
  • Stacey, N.E. and Sorensen, P.W. 2006. Hormonally derived sex pheromones in fish. Chapter 6 in: Fish Reproduction, (ed. K. Pandy), Oxford Press, New Delhi, 201-243.


Progress 01/01/05 to 12/31/05

Outputs
The overarching goal of my research program is to develop an understanding of the role that aquatic chemicals play in lives of fishes so that it may be used to benefit fisheries. I presently have two specific objectives. The first is to determine the identity and function of pheromones (potent chemical signals that pass between organisms of the same species) so that they may ultimately be employed to control nuisance/ invasive species of fish for which few options exist. The second is to determine whether and how endocrine disrupters (chemicals released to the environment that mimic the actions of hormones) influence the reproductive health of fishes. The link between these objectives is that many fish sex pheromones are derived from hormones. I presently have several substantial projects devoted to both objectives which derive considerable supplemental funding from various agencies including the Great Lakes Fishery Commission (lamprey pheromones); Minnesota Sea Grant (endocrine disrupting effects on native minnows); Legislative Commission for Minnesota Resources (common carp);U.S. Fish and Wildlife Service (carp), Australasian Invasive Animal Cooperative Research Centre (common carp), and the Minnesota Department of Natural Resources (carps). Significant progress has been made on all of these projects this past year. The sea lamprey migratory pheromone has now been isolated, structurally elucidated, and found to be comprised of 3 unique disulfated steroids. In collaboration with others, we have also now shown this pheromone will attract migratory sea lamprey in the field at very low concentrations. It is now being developed as a new control strategy and a patent application has been filed. We have also discovered that the common carp releases a species-specific aggregation pheromone that has potential for use in its control. Initial, behavior experiments suggest that bile acids are component of this cue. Support has been garnered to take the next step towards its identification and application. As part of my second objective, my laboratory has discovered that endocrine disrupters with estrogenic actions are found in waters discharged by the Duluth (MN) sewage treatment plant and which reduce the reproductive success of both male and female minnows. The latter effect, never documented to sewage treatment plan effluent before, is especially dramatic and new experiments are presently underway to explain the cause of this important phenomenon.

Impacts
Likely the greatest threat to the fisheries and waterfowl living in the lakes, large rivers, and wetlands of the Upper Midwest are nonindigenous, invasive species, for which no control strategies other than whole-ecosystem poisoning exist. We are making excellent progress towards developing pheromones as a new tool in their management. Similarly, although it clear that pollutants that disrupt hormonal function of fish and wildlife are released by many sewage treatment plants, the precise nature of this threat is as yet obscure. We are finding that the threat is very real but very likely primarily to gene-flow within populations, a finding with insidious ramifications.

Publications

  • Sorensen, P.W., Pinillos, M. Scott, A.P. 2005. Sexually mature male goldfish release large quantities of androstenedione to the water where it functions as a pheromone. General and Comparative Endocrinology 140 (3): 164-175.
  • Fine, J.M., and P.W. Sorensen. 2005. Biologically-relevant concentrations of petromyzonol sulfate, a component of the sea lamprey migratory pheromone, measured in stream waters. Journal of Chemical Ecology 31 (9): 2205-2210.
  • Sorensen, P.W. and Hobson, K.A. 2005. Stable isotope analysis of amphidromous Hawaiian gobies suggest their larvae spend a substantial amount of time in freshwater river plumes. Environmental Biology of Fishes. 74: 31-42.
  • Sorensen, P.W., Fine, J.M., Dvornikovs, V., Jeffrey, C.S., Shao, F., Wang, J., Vrieze, L.A., Anderson, K.R., and Hoye, T.R. 2005. Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nature Chemical Biology 1 (6): 324-328.
  • Stacey, N.E., and Sorensen, P.W. 2005. Hormones, pheromones, and reproductive behaviors. Chapter 9 in: Behaviour: Interactions with Fish Physiology (eds. K.A. Sloman, S. Balshine, and R.W. Wilson), Volume 24 in Fish Physiology (series editors W.S. Hoar, D.J. Randall, and A.P. Farrell). Academic Press.


Progress 01/01/04 to 12/31/04

Outputs
The overarching goal of my research program is to develop a comprehensive understanding of the role of water chemistry in the well being of fishes so that it may be applied to the benefit of our fisheries. I have two objectives. The first is to determine the identity and function of pheromones (potent chemical signals that pass between organisms of the same species) so that they can be employed to control nuisance/ invasive species of fish. The second is to determine whether and how endocrine disrupters (chemicals which mimic the actions of hormones) are influencing the reproductive health of fishes. The link between these topics is that many fish pheromones are derived from hormones. Here I focus on progress understanding fish pheromones which has taken the largest portion of my salary funded by the Agricultural Experiment Station. Pheromones have great promise for use in invasive fish control because they exert powerful effects on fish behavior, are easy and inexpensive to apply, and are environmentally safe. Briefly, funding has been obtained for studies of pheromones in the sea lamprey (Great Lakes Fishery Commission), common carp (Legislative Commission for Minnesota Resources) and Asian carps (U.S. Fish & Wildlife Service). Additionally, I have partnered with the Australasian Invasive Animal Cooperative Research Centre (Canberra, Australia), through which I anticipate receiving funds and significant opportunities for carp control in the future. Significant progress has been made on all projects funded by my efforts. The sea lamprey migratory pheromone has now been isolated, structurally elucidated, and found to be comprised of 3 unique disulfated steroids. This is the first migratory pheromone to identified in a vertebrate. Initial field trials of this pheromone in Michigan have been successful. A patent application has been filed for the use of this pheromone to control lampreys. Other research has demonstrated that common carp release a species-specific aggregation pheromone that has potential for use in control. Support has been garnered to take the next step towards its identification and application. Finally, my lab has discovered evidence that carp use alarm pheromones that might be employed as repellants in invasive fish control. As part of my second objective, my graduate student has discovered that endocrine disrupters with estrogenic actions are found in waters discharged by the Duluth (MN) sewage treatment plant and reduce the reproductive success of native minnows. New funding acquired from Sea Grant should permit further study of androgens found in these effluents. Finally, I have published 6 peer-reviewed publications and given over a dozen talks (three at international forums) based on research supported by Minnesota Agricultural Experiment Station funding.

Impacts
The greatest single threat to the fisheries and waterfowl found in the lakes and large rivers of the Upper Midwest are exotic species. While the common carp (from Europe) may comprise over half the biomass of many shallow lakes where it seriously disrupts benthic food chains through its habit of scavenging in the bottom, the parasitic sea lamprey (from the Atlantic Ocean) kills as many fish as fisherman catch in many areas of the Great Lakes. At present, the only option for controlling these exotic invaders is to poison entire watersheds, an extremely expensive, damaging, and inefficient technique. This project is making good progress towards developing pheromones as a new tool for use as attractants in their management. More recently it has lead to the formation of state (Minnesota Department of Natural Resources), national (U.S. Fish & Wildlife Service, Great Lakes Fishery Commission), and international (Australasian Invasive Animal CRC) networks to promote and employ the approaches it advocates.

Publications

  • Fine, J.M., and P.W. Sorensen. 2004. Mass Spectrometry demonstrates that petromyzonol sulfate, a component of the sea lamprey migratory pheromone, is present in river waters. Advances in Chemical Signals in Vertebrates, eds. Mason, R., D. Muller-Schwarze, Kluwer/ Plenum Press, NY. (in press)
  • 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.
  • Sorensen, P.W., Murphy, C.A., Loomis K., Maniak P., and P. Thomas. 2004. Evidence that 4-pregnen-17,20b,21-triol-3-one functions as a maturation inducing hormone and pheromone precursor in the percid fish, Gymnocephalus cernuus. General and Comparative Endocrinology 139: 1-11.
  • Fine, J.M., Vrieze, L.A., and P.W. Sorensen. 2004. Petromyzontid lampreys appear to employ a common migratory pheromone which is at least partially comprised of bile acids. Journal of Chemical Ecology 30: 2091- 2110.
  • Sorensen, P.W., and K. Sato. 2004. Second messenger systems mediating sex pheromone and amino acid sensitivity in goldfish olfactory receptor neurons. Chemical Senses 29: (in press).
  • Sorensen, P.W., Pinillos, M. Scott, A.P. 2004. Sexually mature male goldfish release large quantities of androstenedione to the water where it functions as a pheromone. General and Comparative Endocrinology 140: (in press)


Progress 01/01/03 to 12/31/03

Outputs
The overarching goal of my research is to develop a comprehensive understanding of the role of water chemistry in the health and well being of fishes. Presently, I have two objectives. One is to determine the identity and function of pheromones (potent chemical signals that pass between organisms of the same species) so that they can be employed to control nuisance/ invasive species of fish. The second is to determine whether and how endocrine disrupters (chemicals which mimic the actions of hormones) are influencing the reproductive health of native fishes. The link between these topics is that many fish pheromones are derived from hormones. First, I address progress understanding fish pheromones. Pheromones have great promise because they are environmentally safe and exert powerful effects on fish behavior and because few options presently exist for the control of the aquatic nuisance species. My laboratory focuses on pheromones employed by the common carp and sea lamprey, the most destructive species in Minnesota. Efforts are also now underway to expand this work to Asian carp which recently invaded Minnesota waters. Following the lead of insect control, we are examining the biochemistry of pheromones and then employed a combination of physiological and behavioral approaches to discern specific function and potency. Using a large flow-through maze with laminar flow equipped with a video digitization system, we have found that both individual and grouped male goldfish (a close relative of the carp which can easily be tested in the laboratory) are strongly attracted to food odor (P<0.05) and that this response persists for up to 15 min. Groups of male goldfish are also attracted to an F prostaglandin-derived sex pheromone, but this response is less long-lived and not seen in individual fishes. This result suggests that social/visual cues are also important in mate location so we have commenced studies that examine the use of both cues. Understanding of the sea lamprey has also progressed significantly during the past year. We have found that the migratory pheromone employed by this species has three components, petromyzonol sulfate, and two, as yet unidentified components, one with a molecular weight of 704, the other 590. The largest component has biological activity at concentrations of 10-14 Molar, a record for fish. We are now attempting to identify it and extract it in quantity so that it can be added to rivers in the spring of 2004 in what promises to be the first ever application of a vertebrate pheromone for pest control. Finally, as part of my second objective we have discovered that endocrine disrupters found in waters discharged by the St. Paul sewage treatment plant significantly reduce the reproductive success of native minnows that are exposed to them for several weeks. Efforts are now underway to elucidate the identity of these compounds and determine their effects over even briefer periods of time.

Impacts
The greatest single threat to the fisheries and waterfowl found in the lakes and large rivers of the Upper Midwest are exotic species. While the common carp (from Europe) may comprise over half the biomass of many shallow lakes where it seriously disrupts benthic food chains through its habit of scavenging in the bottom, the parasitic sea lamprey (from the Atlantic Ocean) kills as many fish as fisherman catch in many areas of the Great Lakes. At present, the only option for controlling these exotic invaders is to poison entire watersheds, an extremely expensive, damaging, and inefficient technique. This project is making good progress towards developing pheromones as a new tool for use as attractants in their management.

Publications

  • Kobayashi, M., P.W. Sorensen, and N.E. Stacey. 2002. Hormonal and pheromonal control of spawning in goldfish. Fish Physiology and Biochemistry 26: 71-84.
  • Rolen, S.H., Sorensen, P.W., Mattson, D., and Caprio, J. 2003. Polyamines as olfactory stimuli in the goldfish, Carassius auratus. Journal of Experimental Biology 206: 1683-1696.


Progress 01/01/02 to 12/31/02

Outputs
The overarching goal of my research is to develop a comprehensive understanding of the identity and function of pheromones (potent chemical signals that pass between organisms of the same species) so that they can be employed to control nuisance and exotic species of fish. This approach has great promise both because pheromones are both environmentally safe and exert powerful effects on fish behavior, and because very few options presently exist for the control of the many nuisance species that ravage our freshwater ecosystems. My laboratory focuses on the common carp and sea lamprey, the most destructive species in Minnesota and elsewhere in the Midwest. During the past year we have conducted studies to determine the complete chemical identities and functions of the pheromones being used by both species. Following the lead of insect control laboratories, we examine the biochemistry of pheromone production and then employed a combination of neurophysiological and behavioral approaches to discern specific function and potency. The past year's studies continue to build on our understanding of how both species employ mixtures of metabolites as potent pheromones whose actions are specific at concentrations in the picomolar range. Using a large flow-through maze with laminar flow and a video digitization system, we found that groups of male goldfish (an immediate relative of the carp which can easily be tested in the laboratory) were strongly attracted to crude food odor (P<0.05) and that this response persists in the absence of a food reward for up to 15 min (P<0.05). Groups of male goldfish were also attracted to an F prostaglandin-derived sex pheromone (P<0.05), but this response was less long-lived than that for the food odor. This result/difference appears attributable to a greater role of visual cues in mate location than in food location as tests using single fish found them less able to locate odor sources when tested in groups, especially the sex pheromone. Accordingly, research has commenced to examine whether visual models of fish might be used in conjunction with pheromones to trap goldfish/carp. Understanding of the sea lamprey has also progressed significantly during the past year. A recently completed fractionation study of the lamprey migratory pheromone has demonstrated that it is comprised of a unique bile acid petromyzonol sulfate and two other components, one with a molecular weight of 590 daltons and the other, 704. We now work to identify them using mass spectrometry. This past summer we also developed means to extract large quantities of the crude pheromone using XAD resins. Finally, we have employed sonically-tags to track free-ranging lamprey as they searched for pheromone in the Great Lakes and found that they can track odor plumes but only do so at night, demonstrating that the pheromone could be used as a lures to enhance riverine captures rates but only if employed in a biologically-relevant manner.

Impacts
The greatest single threat to the fisheries and waterfowl found in the lakes and large rivers of the Upper Midwest are exotic species. While the common carp (from Europe) may comprise over half the biomass of many shallow lakes where it seriously disrupts benthic food chains through its habit of scavenging in the bottom, the parasitic sea lamprey (from the Atlantic Ocean) kills as many fish as fisherman catch in many areas of the Great Lakes. At present, the only option for controlling these exotic invaders is to poison entire watersheds, an extremely expensive, damaging, and inefficient technique. This project is making good progress towards developing pheromones as a new tool for use as attractants in their management.

Publications

  • Grant, G.C., B. Vondracek, and P.W. Sorensen. 2002. Spawning interactions between sympatric brown and brook trout may contribute to species replacement. Transactions of the American Fisheries Society. 131: 569-576.
  • Schoenfuss, H.L., J.T. Levitt, G. VanDer Kraak, and P.W. Sorensen. 2002. Ten week exposure to treated sewage discharge has relatively minor, variable effects on reproductive behavior and sperm production in goldfish. Environmental Toxicology and Chemistry 21: 2185-2190.
  • Stacey, N.E. and P.W. Sorensen. 2002. Fish hormonal pheromones. In: Hormones, Brain, and Behavior. (eds. D.W. Pfaff, D. Arnold, A. Etgen, S. Fahrbach, and R. Rubin). Academic Press. Volume 2, 375-435. Sato, K. and P.W. Sorensen. 2002. Single unit recording from goldfish olfactory receptor neuron using a wide range of biologically relevant odorants suggests high chemospecificity. Chemical Senses. A73. http://www.chemse.oupjournals.org/cgi/data/27/7/661/DC1/1
  • Sorensen, P.W., Caprio, J., Hansen, A., Anderson, K.T., and Finger, T.A. 2002. Differential responsiveness of ciliated and microvillar olfactory receptor neurons in goldfish. Chemical Senses. A75 http://www.chemse.oupjournals.org/cgi/data/27/7/661/DC1/1
  • Hansen, A., Nikonov, A., Anderson, K, Morita, Y., Finger, T., Caprio, J. and Sorensen, P.W. 2002. Functional and biochemical differences between microvillar and ciliated olfactory receptor neurons in catfish. Chemical Senses. A75 http://www.chemse.oupjournals.org/cgi/data/27/7/661/DC1/1


Progress 01/01/01 to 12/31/01

Outputs
The ultimate goal of my research is to develop a comprehensive understanding of the identity and function of pheromones (potent chemical signals that pass between organisms of the same species) so that they can be used in the control of nuisance and exotic species of fish. This approach has great promise because pheromones are both environmentally safe and exert powerful effects on the behavior of many fishes. In addition, few options presently exist for the control of the many nuisance species which ravage our freshwater ecosystems. My laboratory focuses on the common carp and sea lamprey, the most destructive species in Minnesota and elsewhere in the Midwest. During the past year we have conducted studies to determine the complete chemical identities and functions of the pheromones being used by both species. Following the lead of insect control laboratories, we have examined the biochemistry of pheromone production and then employed a combination of neurophysiology and behavior to discern specific function and potency. The past year's studies conclusively demonstrate that both species employ mixtures of metabolites as potent pheromones whose actions are specific and whose threshold is in the picomolar range. We have found that male goldfish (an immediate relative of the carp which can easily be tested in the laboratory) detect and respond to mixtures of three steroids released by females: androstenedione, 17,20b-dihydroxy-4-pregenen-3-one, and, 17,20b-dihydroxy-4-pregenen-3-one-20-sulfate. Further, we have discovered that while individual steroids elicit responses at very low concentrations, when tested as mixtures they synergize (and at times inhibit) each other's actions. These studies have been complimented (and guided by) studies of neural discrimination which are easier to conduct and have identified the presence of mixture -specific neurons. Mixtures should now be considered for use as attractants. Research has also recently commenced using a large maze equipped with a motion analysis system that will allow to define whether or how carp pheromones might function as attractants. Initial results demonstrate that we can attract carp using odorants. Research on sea lamprey has also progressed significantly during the past year. A recently completed fractionation study of the lamprey migratory pheromone has demonstrated that it is comprised of a unique bile acid petromyzonol sulfate (PS) and an as yet unknown component that likely has similar characteristics to PS, from which it may be derived. Consequently, we now focus on this possibility. This past summer we also employed sonically-tags to track free-ranging lamprey as they searched for pheromone in the Great Lakes and found that they do so by performing extensive vertical migrations at night. This is an important finding because it indicates that pheromones should be applied at night and to traps located in rivers whose plumes are deep enough that lamprey. Progress has been substantial and the promise for this approach appears strong as several agencies have offered additional support.

Impacts
The productivity and ecological integrity of Midwestern freshwater ecosystems is severely threatened by a variety of exotic fishes that have been introduced from elsewhere. Sea lamprey and the common carp are of greatest concern, the former in the Great Lakes, the latter in shallow lakes. While the lamprey may take as many fish as fisherman due, the carp through its benthic feeding prevents many lakes from supporting native fishes or even waterfowl. At present, the only option for controlling these exotic invaders is to poison entire watersheds, an extremely expensive, damaging, and inefficient technique. This project is making good progress towards developing pheromones as a new tool for use as attractants in nuisance fish management. Such a tool should save fisheries managers much expense while producing a higher quality resource.

Publications

  • Polkinghorne, C.A., Olson, J.M., Gallaher, D.G., and P.W. Sorensen. 2001. Larval sea lamprey release two unique bile acids to the water at a rate sufficient to produce detectable riverine pheromonal plumes. Fish Physiology and Biochemistry. 24 (1): 15-30
  • Poling, K.R., Fraser, E.J., and P.W. Sorensen, P.W. 2001. The three steroidal components of the goldfish preovulatory pheromone signal evoke different behaviors in males. Comparative Biochemistry and Physiology. Part B. 129: 645-651.
  • Vrieze, L.A., and P.W. Sorensen. 2001. Laboratory assessment of the role of a larval pheromone and natural stream odor in spawning stream localization by migratory sea lamprey. Canadian Journal of Fisheries and Aquatic Science 58: 2374-2385
  • Hanson, L.H. 2001. Coding of pheromonal information in the goldfish olfactory bulb. Ph.D. Dissertation, University of Minnesota, MN.
  • Jared M. Fine 2001. The bile acid derived migratory pheromone employed by sea lamprey is not species-specific. M.S. Thesis, University of Minnesota, MN.
  • Hanson, L.H. and P.W. Sorensen. 2001. Single-unit recording demonstrates that pheromones are discriminated by a combination of labeled-line and combinatorial coding in the goldfish olfactory bulb. Chemical Senses 26(8); abstract #276, p. 1096
  • Poling, K, Hanson, L.H. and P.W. Sorensen. 2001. Behavioral discrimination of sex pheromone mixtures corresponds with physiological profiles of projection neurons. Chemical Senses 26(8); abstract #275, p. 1099
  • Hanson, L.R. and P.W. Sorensen. 2001 Fundamental differences in the processing of pheromonal and non-pheromonal odorants in the goldfish olfactory bulb. Neuroscience Abstracts.


Progress 01/01/00 to 12/31/00

Outputs
The ultimate goal of my research is to establish pheromones, potent chemical signals that pass between organisms of the same species, as a management tool for use in the control of nuisance species of fish. As a first step in this process, I have recently been focusing on determining the complete chemical identities of pheromones in a few species of special interest and ascertaining how potent they might be. This past year we examined pheromones employed by the goldfish and the sea lamprey. The goldfish is used both because it has the best understood pheromone system among the vertebrates and because it is a useful laboratory model which also is closely related to the common carp, a nuisance exotic species. The lamprey is used because it is the most damaging exotic species of fish found in the Great Lakes. This year's studies demonstrate conclusively that both species employ mixtures of various metabolites as potent behavioral pheromones. We have found that male goldfish detect and respond to three steroids: androstenedione which is released largely by males, 17,20b-dihydroxy-4-pregenen-3-one (17,20bP) which is released by ovulatory females, and 17,20b-dihydroxy-4-pregenen-3-one-20-sulfate (17,20bP-S) which is released by ovulating females. We discovered that each steroid elicits distinctive behaviors in males at concentrations below one ten millionth of a gram per liter, the nature of which is strongly modulated when they are tested in natural mixtures. These behavioral actions are complimented by endocrine changes. Especially important is our finding that low concentrations of water-borne androstenedione inhibit responses to the other two steroids, while 17,20bP-S will enhance responses elicited by exposure to 17,20bP. Electrophysiological recording from the goldfish olfactory bulb is also now describing projection neurons that specifically respond to mixtures of these steroids suggesting that the brain is specialized to detect and discriminate particular mixtures of pheromones. Thus, it is now clear that an important goldfish pheromone functions as a mixture. Similarly, a recently completed fractionation study of the lamprey migratory pheromone has clearly demonstrated that it is comprised of two unique bile steroids, petromyzonol sulfate and allocholic acid whose activity is enhanced by at least one other unknown compound. Efforts are presented directed towards determining this unknown component(s). So potent is the entire mixture that larval holding water can attract adult lamprey even when diluted well over 50,000 times and cause a complete reversal in the normal preferences of adult sea lamprey for waters from particular river systems. In conclusion, our studies have now clearly demonstrated the incredible potency and specificity of fish pheromones (and thus their potential for use in management) while providing clear evidence that the complete pheromones are comprised of natural mixtures and given us some direction as to how to isolate and identify the remaining components.

Impacts
The productivity and environmental health of the majority of Midwestern freshwaters ecosystems is threatened by about half a dozen species of exotic species of fish that both reduce watershed productivity and threaten native species of fish. At present, the only option for controlling these exotic invaders is to poison entire watersheds, an extremely expensive, damaging, and often inefficient technique. This project is making good progress towards developing pheromones as a new tool for use as attractants in nuisance fish management. Such a tool should save fisheries managers much expense while producing a higher quality resource.

Publications

  • BJERSELIUS, R., LI, W., TEETER, J.H., SEELYE, J.G., MANIAK, P.J., GRANT, G.C., POLKINGHORNE, C.N. and P.W. SORENSEN. 2000. Direct behavioral evidence that unique bile acids released by larval sea lamprey function as a migratory pheromone. Canadian Journal of Fisheries and Aquatic Sciences 57: 557-569.
  • SORENSEN, P.W., SCOTT, A.P., and KIHSLINGER, R.L. 2000. How common hormonal metabolites function as specific pheromones in the goldfish. IN: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish, eds. B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson, and S.O. Stefansson, Bergen, Norway, 125-128.
  • MANIAK, P.J. LOSSING, R., and P.W. SORENSEN. 2000. Injured Eurasian ruffe, Gymnocephalus cernuss, release an alarm pheromone which may prove useful in their control. Journal of Great Lakes Research 26(2): 183-195.
  • SORENSEN, P.W., and J. CAPRIO. 2000. Restricted distribution and chemospecificity of pheromone-sensitive olfactory receptor neurons in the goldfish olfactory epithelium. Chemical Senses. 25(5) 670.
  • HANSON, L.H., COHEN, Y. and SORENSEN, P.W. 2000. Identified pheromones evoke distinctive spatial maps of activity that are independent of concentration in the goldfish olfactory bulb. Chemical Senses. 25(5) 607.
  • POLING, K.R., and SORENSEN, P.W. 2000. Individual components of the goldfish pre-ovulatory pheromone elicit different behavioral responses: the first step in understanding the role of mixtures in a vertebrate pheromone. Chemical Senses. 25(5) 602.
  • SPECA, D.J., LIN, D.M., SORENSEN, P.W., ISACOFF, E.Y., NGAI, and DITTMAN, A.H. 2000. Molecular characterization of odorant receptors from fish. Chemical Senses. 25(5) 636.


Progress 01/01/99 to 12/31/99

Outputs
Significant progress has been made understanding the reproductive biology of cyprinid fishes and the role of hormonal sex pheromones in determining fertility in fishes. Although our primary goal remains to establish pheromones as a tool for the management of nuisance fish species, the fundamental role of these cues in mediating various behavioral and physiological responses in fishes has allowed us to expand into 5 areas. Our research continues to center on the goldfish because it has the best understood pheromone system among the vertebrates and a useful laboratory model that is closely related to the common carp, a nuisance exotic species. First, we have confirmed earlier studies suggesting that male goldfish perceive and respond to identified pheromonal stimuli within the context of the body odor within which they are normally found. In particular, we find that responsiveness of goldfish to pheromonal components is blocked when the latter are administered together with heterospecific body odor. Further, we have found that bile acids are part of this body odor perceived by goldfish. This finding is significant because it demonstrates that fish sex pheromones, like those used by insects, are likely complex mixtures and may be species-specific when found (and applied) in appropriate odor contexts. Second, we have identified specific neural pathways within the goldfish system that are specialized for the perception of pheromonal cues. This knowledge provides us with a means of assessing the identities of pheromone mixtures and how they might be manipulated for biocontrol. Third, in related work on the sea lamprey (the most destructive exotic fish pest of the Great Lakes), we have shown that their bile acid pheromone is part of a more complex pheromonal mixture. We are working toward elucidating the components of that pheromonal mixture. Additionally, we have nearly completed work developing an immunoassay that will enable us to routinely measure the lamprey pheromone in natural river waters, thereby providing an inexpensive tool to estimate sea lamprey abundance. Fourth, we have clearly demonstrated endemic freshwater gobies of the Hawaiian Islands rely on migratory pheromone attractants to locate fresh water, demonstrating that ongoing efforts to conserve these populations must improve water quality and ecosystem health as well as increase absolute flow rates. Fifth, we have started a study to elucidate the effects of endocrine disrupting compounds (EDCs) found in the St. Paul sewage treatment plant on the fertility of male goldfish. Because of our research on goldfish reproductive behavior, this species has become an excellent laboratory model for such studies and we plan to use it to study EDCs in several locations in Minnesota.

Impacts
(N/A)

Publications

  • SORENSEN, P.W., & STACEY N.E. 1999. Evolution & specialization in fish hormonal pheromones. Adv. in Chem. Signals in Vertebrates, Eds. Johnston, Muller-Schwarze & Sorensen, Plenum Press. 15-48.
  • STACEY, N.E., & P.W. SORENSEN. 1999. Pheromones, Fish. In: Encyclopedia of Reproduction, Volume 3, Eds. E. Knobil & J.D. Neill, Academic Press, N.Y. pp.748-755.
  • JOHNSTON, R.E., MULLER-SCHWARZWE, D & P.W. SORENSEN. 1999. (Editors) Advances in Chemical Signals in Vertebrates, Plenum Press, NY. 674pp.
  • HANSEN, A., ZIPPEL, P.H., SORENSEN, P.W., & J. CAPRIO. 1999. The ultrastructure of the olfactory epithelium in intact, axotomized & bulbectomized goldfish. Microscopy Res. & Tech. 45: 325-338.
  • SPECA, D.J., LIN, D.M., SORENSEN, P.W., ISACOFF, E.Y., NGAI, & DITTMAN, A.H. 1999. Functional identification of a goldfish odorant receptor. Neuron 23: 487-498.
  • KIHSLINGER, R.L., & P.W. SORENSEN. 1999. Pheromonal cues in the goldfish are perceived within the context of the body odor within which they occur. Chem. Senses 24 (5): abstract 342, p.616.
  • HANSON, L.H., CAPRIO. J., & SORENSEN, P.W. 1999. Pheromone-sensitive mitral cells in the goldfish respond to more than one odotope. Chemical Senses 24 (5): abstract#164, p.567.
  • APPELT, C.W., & P.W. SORENSEN 1999. Freshwater fish release urinary pheromones in a pulsatile manner. Advan. in Chem. Signals in Vertebrates, Eds.Johnston, Muller-Schwarze & Sorensen, Plenum Press. 247-256.


Progress 01/01/98 to 12/31/98

Outputs
Our understanding of how pheromones control the behavior of fishes has advanced significantly over the past year as a direct result of four studies conducted within the context of this project. Our ultimate goal is to establish pheromones as a new tool for the management of nuisance fish species. Much of the present work has centered on the goldfish both because it has the best understood pheromone system among the vertebrates and because it is a useful laboratory model which is closely related to the common carp (a nuisance exotic species). First, in a series of behavioral experiments we have discovered that the male goldfish perceives and responds to identified pheromonal stimuli within the context of the body odor within which these stimuli are normally found. Thus, behavioral responses of goldfish to identified pheromonal components are blocked when the latter are administered together with the body odor of heterospecifics. This finding is significant because it demonstrates that fish sex pheromones, like those used by insects, are likely complex mixtures and may be species-specific when found in appropriate odor contexts - and can be used in control. Second, and building on the former finding, we are starting to discern the physiological (neural) basis by which such complex odors are recognized by the goldfish, and likely other fish. Such an understanding should eventually allow us to discern what these mixtures are and how they might be manipulated for biocontrol. Specifically, we have used electrophysiological recording to discover that at least some of the olfactory glomeruli in the goldfish olfactory bulb, like that of the insect, detect both pheromonal cues and other stimuli found in fish body odor. This discovery also demonstrates that more than one class of odorant receptor molecule is expressed on individual olfactory receptor neurons. Third, in related work on the sea lamprey (the most destructive exotic fish pest of the Great Lakes), we have now shown that their bile acid pheromone (which was identified in connection with this project) is also released by native lamprey species, suggesting the latter may be used as source of pheromonal odor to control the former. Additionally, we have developed an antibody technique which will soon enable us to routinely measure the lamprey pheromone in natural river waters, thereby providing inexpensive tool to estimate sea lamprey abundance. Fourth, we have discovered that the major freshwater fish fauna of the Hawaiian islands rely on migratory pheromone attractants, demonstrating that ongoing efforts to conserve these populations must improve water quality and ecosystem health as well as increase absolute flow rates. Many publications are in preparation and our work has received a great deal of attention from many fisheries management agencies and related groups.

Impacts
(N/A)

Publications

  • Hanson, L.R., Sorensen, P.W., and Y. Cohen. 1998. Sex pheromones and amino acids evoke distinctly different patterns of electrical activity in the goldfish olfactory bulb. Olfaction and Taste XII An International Symposium. Annals of the New York Academy of Sciences, ed. C. Murphy, NY, NY. 521-524.
  • Sorensen, P.W., T..A. Christensen, and N.E. Stacey. 1998. Discrimination of pheromonal cues in fish: emerging parallels with insects. Current Opinion in Neurobiology 8(4): 458-467.
  • Essington, T.E., P.W. Sorensen, and D.G. Paron. 1998. Redd superimposition in stream resident brook trout (Salvelinus fontinalis) and brown trout (Salmo trutta) cannot be explained by habitat alone. Canadian Journal of Fisheries and Aquatic Sciences. 55: 2310-2316.
  • Sorensen, P.W., and J. Caprio. 1998. Chemoreception in fish. Chapter 15 In: The Physiology of Fishes, second edition, ed. R.E. Evans, CRC Press, FL., pp. 375-406.


Progress 01/01/97 to 12/31/97

Outputs
Our understanding of pheromonal control of behavior in fishes was advanced by several studies connected with this project. First, continuing our investigation of how specialized fish pheromones might be, we have elucidated specific regions of the goldfish olfactory bulb (brain) which are dedicated to processing both sex and bile steroid pheromones. Because these brain regions are discrete and do not overlap, it seems likely that fish are capable of deciphering complex mixtures of pheromonal components. This scenario is also indicative of a `complex labeled line' such as used by those insects, and for which a comprehensive understanding has helped design effective pheromonal attractants. Second, we have now elucidated that female goldfish control modulate urinary pheromone release, so that this signal has a significant temporal component. Clearly, when these cues are applied to the management of wild pest species of fish they should be pulsed in an appropriate manner and context. Third, related work on both the sea lamprey and Eurasian ruffe, exotic pests of considerable importance to the fisheries of the Great Lakes, appears to be confirming these suppositions and providing the first practical demonstrations of the utility of pheromones. We have now succeeded in attracting adult sea lamprey to pulsated mixtures of two conspecific bile acids (pheromones). Also, we have succeeded in demonstrating that the ruffe can be repulsed using skin pheromone extracts liberated from their skin. The latter phenomenon may prove useful in keeping ruffe from entering the Mississippi River via the Chicago Ship canal.

Impacts
(N/A)

Publications

  • Zippel, H.P., P.W. Sorensen, and A. Hansen. 1997. High correlation between microvillous receptor cell abundance and sensitivity to pheromones in olfactory nerve-sectioned goldfish. Journal of Comparative Physiology A. 180: 39-52.
  • Li, W., and P.W. Sorensen. 1997. Highly independent olfactory receptor sites for conspecific bile acids in the sea lamprey, Petromyzon marinus. Journal of Comparative Physiology A. 180(4): 429-438.
  • Hanson, L.R., Sorensen, P.W., and Y. Cohen. 1997. Sex pheromones and amino acids evoke distinctly different patterns of electrical activity in the goldfish olfactory bulb. Proceedings of the International Symposia on Olfaction and Taste XII, New York Academy of Sciences, ed. C. Murphy., NY, NY. (in press)
  • Sorensen, P.W., and J. Caprio. 1997. Chemoreception in fish. Chapter 15 In: The Physiology of Fishes, second edition, ed. R.E. Evans, CRC Press, FL., pp. 375-406.


Progress 01/01/96 to 12/30/96

Outputs
Good progress was made understanding hormonal and pheromonal control of sexual behavior in fishes. We made two important findings. First, we discovered that female goldfish control the release of behaviorally-active pheromones by altering their urinary release. In particular, female goldfish release urine more frequently when sexually-active and in the immediate presence of spawning substrate. Thus, fish pheromonal signals may have a visual and temporal component. When these cues are applied to the management of wild pest species of fish (such as common carp, an exotic pest) they should be pulsed in an appropriate manner and context. Second, we discovered that the olfactory sensitivity of goldfish to pheromonal odorants is associated with a distributed network of neurons which projects across the surface of their olfactory bulb. This scenario is indicative of a complex labeled line such as used by those insect species which employ multi-component pheromonal signals. Thus, signal complexity and species-specificity should be considered in future studies of pheromonal function in fishes. Related work on sea lamprey and Eurasian ruffe, exotic pests of considerable importance to the fisheries of the Great Lakes, continues to make good progress and uses many of the techniques developed for the goldfish.

Impacts
(N/A)

Publications

  • BJERSELIUS, B., W. LI, and P.W. SORENSEN. 1996. Spermiated male sea lamprey release a potent sex pheromone. In: Proc. of the Fifth International Symp. on the Reproductive Physiology of Fish, eds. F. Goetz & P. Thomas, Fish Symp. 95, Austin, APPELT, C., P.W.
  • SORENSEN, and R.G. KELLNER. 1996. Female goldfish appear to release pheromonally active F-prostaglandins in urinary pulses. In: Proc. of theFifth International Symp. on the Reproductive Physiology of Fish, eds. F. Goetz & SORENSEN, P.
  • W., A.R. BRASH, F.W. GOETZ, R.G. KELLNER, L. BOWDIN, and L.A. VRIEZE. 1996. Origins and functions of F prostaglandins as hormones and pheromones in the goldfish. In: Proc. of the Fifth International Symp. on the Reproductive Phy CARDWELL, J.
  • R., P.W. SORENSEN, G.P. VANDERKRAAK, and N.R. LILEY. 1996. Effect ofdominance status on sex hormone levels in laboratory and wild-spawning male trout. Gen. & Compar. Endocrinology. 101(3):333-341.
  • ESSINGTON, T. E., and P.W. SORENSEN. 1996. Overlapping sensitivities of brook trout and brown trout to putative hormonal pheromones. J. of Fish Biol. 48:1027-1029.
  • SORENSEN, P.W. 1996. Behavioral responsiveness to pheromones provides fundamental and unique insight into olfactory function. Chemical Senses. 21(2)2.


Progress 01/01/95 to 12/30/95

Outputs
Good progress was made understanding hormonal & pheromonal control of sexual behavior in fishes. Our principal finding was the elucidationof pheromone release pathways & rates. Using both radioactive tracers & dye, we have confirmed our previous biochemical studies which suggested that behaviorally active pheromones are exclusively released via the urine. Furthermore, we have discovered that urinary release is pulsative and perhaps under female control. This raises the possibility that pheromonal cues have a temporal component, in other words, exposure/release rate is critical to cue function. If this is in fact the case (experiments are underway to ascertain this possibility), then measures directed towards the application of pheromones in the management of wild pest species of fish will have to pulse signals to optimize their potential utility. Another significant finding was our elucidation & identification of a steroidalpheromone released by spawning male goldfish which has inhibitory actions on conspecific reproductive physiology. Because this cue is also likely used by common carp, an exotic pest, it may have applications. Related work on sea lamprey continues to make good progress & uses many of the techniques developed for the goldfish.

Impacts
(N/A)

Publications

  • PALMER, E.E., ET. AL. 1995. A histological study of seasonal ovarian development in freshwater drum in the Red Lakes, MN. J. Fish Biol. 47: 199-210.
  • LI, W. ET.AL. 1995. The olfactory system of migratory adult sea lamprey is specifically & acutely sensitive to unique bile acids released by conspecific larvae. J. of Gen. Phys. 105: 569-589.
  • SORENSEN, P.W., ET. AL. 1995. Sulfated, 17,20B-dihydroxy-4-pregnen-3-one functions as a potent & specific olfactory stimulant with pheromonal actions in the goldfish. Gen. Comp. End. 100(1):128-142.
  • SORENSEN, P.W., ET. AL. 1995. Reproductive interactions between brook & brown trout in a small MN stream. CJFAS. in-press.
  • CARDWELL, J.R., ET. AL. 1995. Effect of dominance status on sex hormone levels in laboratory & wild-spawning male trout. Gen. & Comp. Endoc. IN PRESS.
  • ESSINGTON, T.E. AND P.W. SORENSEN. 1995. Overlapping sensitivities of brook trout & brown trout to putative hormonal pheromones. J. Fish. Biol. IN PRESS.
  • BJERSELIUS, R., W. LI, AND P.W. SORENSEN. 1995. Spermiated male sea lamprey release a potent sex pheromone. Proc. of Fifth Internat. Symp. Reprod. Phys. of Fish. in-press.
  • APPELT, C., P.W. SORENSEN, AND R.G. KELLNER. 1995. Female goldfish appear to release pheromonally active F-prostaglandins in urinary pulses. Proc. Fifth Intern. Symp. Reprod. Phys. of Fish. IN PRESS.


Progress 01/01/94 to 12/30/94

Outputs
Good progress was made understanding hormonal and pheromonal control behavior infishes. We continue to build towards the point when we can use these cues to control and monitor populations of wild fish. First, we confirmed that prostaglandin F2a (PGF2a) is responsible for the expression of female sexual behavior and serves as the precursor of the spawning pheromone. This was done by tracing its levels and fates in sexually active female goldfish. This finding is important because this compound is the precursor for spawning pheromones in many species of fish. Second, we have found that fish metabolize this important hormone by conjugating it with glucose. Third, we discovered that pheromonally-active metabolites of PGF2a are released in the urine, a pathway which fish can control -- and we must thus mimic in bio-control strategies. Fourth, we found that spawning male goldfish produce and release great quantities of an inhibitory pheromone, androstenedione. Together these findings greatly increase our understanding of how pheromones are produced, released, and perceived: building towards technologices which might be useful in the control of wild fishes.

Impacts
(N/A)

Publications

  • LI, W. 1994. The olfactory biology of adult sea lamprey. Ph.D. Thesis. U. of MN.
  • LI, W.M., AND P.W. SORENSEN. 1994. High specificity of the sea lamprey olfactory system to four classes of bile acids. Chem. Senses 19(5) Abstracts #165. P. 506.
  • SORENSEN, P.W. 1994. Effect of electroshocking on the sexual behavior of goldfish & brook trout. NAJF Manage. 14: 862-865.
  • SORENSEN, P.W., AND L. BOWDIN. 1994. Olfactory responsiveness of female goldfish to sex pheromones ........ Chem. Senses 19(5) Abs. 278 P. 555-556.
  • SORENSEN, P.W. AND L. HANSON. 1994. Luring lampreys: Assessing the feasibility of using natural odorants to control sea lamprey in the Great Lakes. Wkshp. Proceedings sponsored by GLFC. 110 p.
  • SORENSEN, P.W. AND A.P. SCOTT. 1994. The evolution of hormonal sex pheromones in teleost fish: Poor ...... Acta Scandinavia Physiologica 152:19-205.
  • STACEY, NE., J.R. CARDWELL, N.R. LILEY, A.P. SCOTT, AND P.W. SORENSEN. 1994. Hormones as sex pheromones in fish. IN: K.G. Davey, et al. (eds.) Perspect. in Comp. Endocr. Nat. Res. Council of Canada, p. 438-448.
  • WEIGEL, D.E. 1994. Physical & biological correlates of the distribution of sympatric populations of brook, brown, & rainbow trout in Valley Creek, MN. MS Thesis. U. of MN.
  • ZIPPEL, H.P. AND P.W. SORENSEN. 1994. Olfactory respons. to amino acids & sex pheromones returns ....... Chemical Senses 19(5) Abs. 335, P. 580.


Progress 01/01/93 to 12/30/93

Outputs
Significant progress was made in understanding the production, release and identity of the prostaglandin-derived sex pheromones used by goldfish and other fishes. First, we have confirmed that prostaglandin F(2a) (PGF(2A)) is the precursor of the spawning pheromone by using radioimmunoassay and mass spectrometry to positively identify it in the blood of ovulated goldfish and then establish that its production increases nearly 50 fold during the course of ovulation when pheromones are known to be released. This is particularly significant because this is the first chemical confirmaton of this compound in a fish and the plasma levels measured (15ng/ml) are the highest reported in a vertebrate. Second, using a radio-labeled tracer we have established that PGF(2a) is rapidly cleared from the blood of goldfish (within minutes) and released via the urine to the water as a mixture of five novel metabolites, two of which have pheromonal function. One of the pheromonally-active metabolites (15-keto-PGF(2A)) is released at the unprecedented rate of 500 ng/h. Third, the olfactory sensitivity of fish to these metabolites is sexually dimorphic and species-specific. Fourth, studies of the metabolism of PGF(2a) in other fish suggests that other fish may produce other metabolites: the prostaglandin pheromone may be species-specific.

Impacts
(N/A)

Publications

  • DEFRAIPONT, M. and SORENSEN, P.W. 1993. Exposure to the pheromone 17a,20b-dihydroxy-4-pregnen-3-one enhances the behavioural spawning success, sperm production and sperm motility of male goldfish. Animal Behaviour 46: 245-256.
  • SORENSEN, P.W. and GOETZ, F.W. 1993. Pheromonal function of prostaglandin metabolites in teleost fish. Journal of Lipid Mediators 6: 385-393.
  • IRVINE, I.A. and SORENSEN, P.W. 1993. Acute olfactory seniitivity of wild common carp, Cyprinus carpio, to goldfish hormonal pheromones is influenced by gonadal maturity. Canadian Journal of Zoology 71: (in-press).
  • LI, W.M., SORENSEN, P.W. and GALLAHER, D.D. 1993. The olfactory system of sea lamprey is highly sensitive and specific to bile acids produced by fish. Chemical Senses 18(5) abstract (in press).


Progress 01/01/92 to 12/30/92

Outputs
IDENTIFICATION AND FUNCTIONAL CHARACTERIZATION OF SEX PHEROMONE FUNCTION IN CYPRINID FISH Our investigation of the reproductive biology of common carp, CYPRINUS CARPIO, was concluded and the student responsible for this project defended his thesis (Irvine, 1992). These data are now being prepared for publication. Larval abundance and gonadal maturity of wild common carp collected from the Mississippi River were correlated with water temperature, river height and rainfall between 1984 and 1991 to determine their effects on the timing of reproduction. When water temperature was above 15(degree)C spawning was strongly correlated with periods of elevated river stage but not rainfall. Flooded vegetation is likely required for spawning and may function as a reproductive trigger in the spring. The olfactory responsiveness of wild carp to putative steroidal pheromonal was also measured by electro-olfactogram (EOG) recording. Of 33 sex steroids tested, 17(alpha),20(beta)-dihydroxy-4-pregnen-3-one (17,20P) was the most stimulatory. It had a detection threshold of 10(superscript -13) Molar (M). EOG responsiveness also indicated a high degree of sensitivity and specificity to both 17,20P-sulfate (17,20P-S; a novel metabolite (Sorensen & Scott 1992)), and to the C19 steroid, androstendione. The EOG responses of juvenile carp to 10(superscript -8) M androstendione were greater than those of adults.

Impacts
(N/A)

Publications

  • IRVINE, I.A.S. 1992. Reproductive biology of the common carp (Cyprinus carpio) in Minnesota: Olfactory sensitivity to putative sex pheromones and environmental influences on spawning. Unpublished Master's Thesis, University of Minnesota.
  • LI, W.M. and P.W. SORENSEN (1992). The olfactory sensitivity of sea lamprey to amino acids is specifically restricted to arginine. Chemical Senses 17(5), abstract #163, p.658.
  • SORENSEN, P.W., and A.P. SCOTT (1992). Sulfated sex steroids: A new class of olfactory stimulants with pheromonal actions in teleost fish. Chemical Senses 17(5), abstract #259, p. 700.
  • SORENSEN, P.W. 1992. Hormones, pheromones, and chemoreception. Chapter 10 In: Fish Chemoreception, ed. T.J. Hara, Chapman and Hall, London, pp. 199-228.
  • SORENSEN, P.W. 1992. Hormonally-derived sex pheromones in goldfish: A model for understanding the evolution of sex pheromone systems in fish. Biological Bulletin 183: 173-177.


Progress 01/01/91 to 12/30/91

Outputs
Our investigation of the potential involvement of sex pheromones in carp, Cyprinus carpio, reproduction continued. Once again wild carp captured monthly from May-October and their gonadal development measured. Last year's findings were confirmed. Analysis of carp larval abundance data now show that spawning events are synchronized by temperature and photoperiod and triggered by rising water levels. Last years electro-olfactogram (EOG) data were also confirmed and extended to include more compounds. These data have been partitioned to analyze seasonal changes in responsiveness. At least two classes of steroid olfactory receptor mechanisms were shown to be present in the carp olfactory system using cross-adaptation techniques. One is highly sensitive and specific to 17a,20beta-dihydroxyprogesterone (17,20P) and the other is sensitive to androgenic steroids. Mature males were found to detect 17,20P with greater sensitivity than either mature females and young of the year (YOY) fish of either sex. Conversely YOY fish and mature females were more sensitive to androstenedione. Pheromones appear to have potential for biocontrol in this species and a preliminary bioassay of mature male carp responsiveness to pheromonal 17,20P was conducted to address this possibility. Free swimming carp exposed to 17,20P produced a greater volume of milt than control fish. Blood samples are being analyzed for circulating hormones. Data are currently being statistically analyzed and written up for publication.

Impacts
(N/A)

Publications


    Progress 01/01/90 to 12/30/90

    Outputs
    Significant progress has been made towards identifying sex pheromones used by the carp, Cyprinus carpio. The first systematic study of the reproductive biology of wild carp in North America is also underway. These findings make a fundamental contribution towards understanding the reproductive biology of fish and provide tools for both promoting carp reproduction in third world aquaculture and suppressing it in North America. Wild carp were captured monthly from May-October, their gonadal development measured and olfactory sensitivity to steroidal hormones determined by electro-olfactogram recording (EOG). Carp appear to spawn in discrete surges between May and July suggesting pheromonal synchronization of reproduction. The carp olfactory system is extremely sensitive to the steroid, 17(alpha), 20(beta)20dihydroxyprogesterone (17,20P) which it detects at concentrations approaching 10(superscript -13 ) Molar (1 gram in 30 billion liters). EOG responsiveness is similar to that of the goldfish, a species it hybridizes with to produce infertile offspring. The carp olfactory system also detects androgenic steroids which have been suggested to function as inhibitory pheromones in goldfish; sensitivity to these compounds increased in August. Electrophysiological monitoring of olfactory sensitivity will continue in 1991 to confirm these results verify that the EOG reflects responses conveyed centrally, and determine whether maturity influences olfactory acuity.

    Impacts
    (N/A)

    Publications

    • SORENSEN, P.W., T.J. HARA, N.E. STACEY, and J.G. DULKA. 1990. Extreme olfactory specificity of male goldfish to the preovulatory pheromone 17 ,20 -dihydroxy-4-pregnen-3-one. Journal of Comparative Physiology A. 166(3):373-385.
    • STACEY, N.E. and P.W. SORENSEN. 1990. Identified sex pheromones in fish: endocrine and behavioral effects. In. Fish Physiology, Fish Toxicology, and Fisheries Management: Proceedings of an International Symposium, Guangzhou, Peoples Repub.


    Progress 01/01/89 to 12/30/89

    Outputs
    This project started approximately 3 months ago and two lines of investigation have commenced: 1) Behavioral effects of the preovulatory steroidal pheromone 17 alpha, 20 beta-dihydroxy-4-pregnen-3-one (17 alpha, 20 beta P) on mature male goldfish, Carassius auratus. Although it is established that female goldfish release 17 alpha, 20 beta P and males detecting it experience dramatic increases in gonadotropic hormone and milt production, the behavioral effects of this pheromone are unknown. Initial experiments have found that male goldfish exposed to 17 alpha, 20 beta P 8 hours prior to spawning spawn approximately 5 times more frequently than control males not exposed to this pheromone. Additionally, pheromone-exposed males have larger volumes of milt and their sperm is more motile. 2) Investigations of the possibility that steroidal pheromones might be species-specific. Electrophysiological examination of the olfactory sensitivity of the hornyhead chub, Nocomis biguttatus to progestational steroids has started. Interestingly, this species (which is cultured for use as a baitfish in Minnesota) appears to be acutely sensitive to 17 alpha, 20 beta dihydroxy-4-pregnen-3-one glucuronide, a metabolite of 17 alpha, 20 beta P which goldfish do not detect; this is the first indication that fish may commonly use sex hormones as pheromones and that differences in metabolism may cause pheromones to be species-specific.

    Impacts
    (N/A)

    Publications

    • SORENSEN, P.W., STACEY, N.E. and CHAMBERLAIN, K.J. 1989. Differing behavioral and endocrinological effects of two female sex pheromones on male goldfish. Hormones and Behavior 23: 317-332.