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REVIEW

Carp chemical sensing and the potential of natural environmental attractants for control of carp: a review

Aaron Elkins A B , Russell Barrow B and Simone Rochfort A C
+ Author Affiliations
- Author Affiliations

A Biosciences Research Division, Department of Primary Industries, Victoria, 1 Park Drive, La Trobe University, Vic. 3083, Australia.

B Research School of Chemistry, Australian National University, Canberra, ACT 0200, Australia.

C Corresponding author. Email: simone.rochfort@dpi.vic.gov.au

Environmental Chemistry 6(5) 357-368 https://doi.org/10.1071/EN09032
Submitted: 10 March 2009  Accepted: 25 August 2009   Published: 22 October 2009

Environmental context. Carp are responsible for causing significant damage to lakes and rivers resulting in highly turbid water impacting native fish. At present there are no effective ways to manage the damage caused by carp or eradicate them, but the efficiency of carp removal from our waterways can be enhanced by the development of naturally occurring environmental attractants. As part of a broader pest management scheme the implementation of these attractants can significantly enhance the effectiveness of eradication programs and lead to the restoration of our waterways.

Abstract. Cyprinus carpio, a species of carp commonly known as European or common carp, are invasive alien species in Australian inland waters and have an extensive impact on biodiversity and the aquatic environment. The control and eradication of carp is a major focus of fisheries services throughout Australia, but at present there is no wholly successful way to limit the damage caused. An integrated pest management scheme (IPM) is the most likely approach to be effective. Such a scheme could employ current tactics such as trapping in combination with new strategies including attractants or deterrents. Among proposed attractants are environmentally derived chemicals. Carp have long been observed to prefer certain habitats and environmental conditions over others, although the reasons for such a preference are not well defined. This article reviews the current scientific literature for chemical reception and attraction in carp with an emphasis on environmentally derived attractants and the potential for use of these chemical cues to enhance IPM strategies with minimal environmental impact.

Additional keywords: analysis, attraction, chemical ecology, chemoreception, environment, pest management, pheromones, synthesis.


Acknowledgements

The authors acknowledge the financial support of the Invasive Animals Cooperative Research Centre (IA CRC) in formulating this review, the Victorian Department of Primary Industries for the use of their facilities and resources and the Australian National University granting a postgraduate award for the research to be conducted.


References


[1]   Barnham C., Carp in Victoria, in D.o.P. Industries, edn FN0014 (Ed. Fisheries Victoria) 2007.

[2]   Gardner C., A Little Carp History, in History of Common Carp 2007. Available at http://www.environment-agency.gov.uk/subjects/fish/246986/342184/578061/578109/ [Verifed 19 June 2007]

[3]   Q.-G. Liu , Y. Chen , J.-L. Li , L.-Q. Chen , The food web structure and ecosystem properties of a filter-feeding carps dominated deep reservoir ecosystem. Ecol. Modell. 2007 , 203,  279.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[4]   P. Brown , T. I. Walker , CARPSIM: stochastic simulation modelling of wild carp (Cyprinus carpio L.) population dynamics, with applications to pest control. Ecol. Modell. 2004 , 176,  83.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[5]   D. C. Hockin , K. O’Hara , J. W. Eaton , A radiotelemetric study of the movements of grass carp in a British canal. Fish. Res. 1989 , 7,  73.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[6]   Inland Fisheries S., Carp Annual Report 05–06 2005 (Inland Fisheries Service: Hobart).

[7]   P. W. Sorensen , N. E. Stacey , Brief review of fish pheromones and discussion of their possible uses in the control of non-indigenous teleost fishes. N. Z. J. Mar. Freshw. Res. 2004 , 38,  399.
         open url image1

[8]   J. R. Pawlik , Chemical induction of larval settlement and metamorphosis in the reef-building tube worm Phragmatopoma californica (Sabellariidae: Polychaeta). Mar. Biol. 1986 , 91,  59.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[9]   R. A. Gleeson , Morphological and behavioural identification of the sensory structures mediating pheromone reception in the blue crab, Callinectes sapidus. Biol. Bull. 1982 , 163,  162.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[10]   A.-S. Krång , S. P. Baden , The ability of the amphipod Corophium volutator (Pallas) to follow chemical signals from con-specifics. J. Exp. Mar. Biol. Ecol. 2004 , 310,  195.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[11]   D. Rittschof , Chemical attraction of hermit crabs and other attendants to simulated gastropod predation sites. J. Chem. Ecol. 1980 , 6,  103.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[12]   M. J. Weissburg , R. K. Zimmer-Faust , Life and death in moving fluids: hydrodynamic effects on chemosensory-mediated predation. Ecology 1993 , 74,  1428.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[13]   L. M. Samuelsson , L. Forlin , G. Karlsson , M. Adolfsson-Erici , D. G. J. Larsson , Using NMR metabolomics to identify responses of an environmental estrogen in blood plasma of fish. Aquat. Toxicol. 2006 , 78,  341.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[14]   M. G. Pawson , Analysis of a natural chemical attractant for whiting Merlangius merlangus L. and cod Gadus morhua L. using a behavioural bioassay. Comp. Biochem. Physiol. A 1977 , 56,  129.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[15]   Pacific Northwest Laboratories, Final Report on Chemical Attractants for the Carp, Cyprinus carpio, in Battelle Memorial, 31 May 1967.

[16]   Y. Ishida , H. Yoshikawa , H. Kobayashi , Electrophysiological responses of three chemosensory systems in the carp to pesticides. Physiol. Behav. 1996 , 60,  633.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[17]   K. M. Ferrari , N. M. Targett , Chemical attractants in horseshoe crab, Limulus polyphemus, eggs: the potential for an artificial bait. J. Chem. Ecol. 2003 , 29,  477.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[18]   K. Ide , K. Takahashi , K. Sasaki , M. Omori , Predation by scavenging amphipods to injured hatchery-raised juvenile Japanese flounder Paralichthys olivaceus under laboratory conditions. Fish. Sci. 2006 , 72,  1209.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[19]   K. Harada , S. Maruyama , K. Nakano , Feeding attractants in chemical constituents of brown alga for young abalone. Nippon Suisan Gakkai Shi 1984 , 50,  1541.
         open url image1

[20]   K. Harada , H. Matsuda , Feeding attractants in chemical constituents from the mid-gut gland of squid for juvenile yellowtail. Nippon Suisan Gakkai Shi 1984 , 50,  623.
         open url image1

[21]   K. Harada , I. Ikeda , Feeding attractants in chemical constituents of lake prawn for oriental weatherfish. Nippon Suisan Gakkai Shi 1984 , 50,  617.
         open url image1

[22]   W. E. S. Carr , J. C. Netherton , R. A. Gleeson , C. D. Derby , Stimulants of feeding behavior in fish: Analyses of tissues of diverse marine organisms. Biol. Bull. 1996 , 190,  149.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[23]   P. Saglio , B. Fauconneau , J. M. Blanc , Orientation of carp, Cyprinus carpio L., to free amino acids from Tubifex extract in an olfactometer. J. Fish Biol. 1990 , 37,  887.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[24]   Pfeiffer W., Chemical signals in communication, in Chemoreception in fishes 1982, pp. 307–326 (Elsevier: New York).

[25]   W. E. S. Carr , E. R. Hall , S. Gurin , Chemoreception and the role of proteins: A comparative study. Comp. Biochem. Physiol. Part A. Physiol. 1974 , 47,  559.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[26]   E. H. Hamdani , G. Alexander , K. B. Døving , Projection of sensory neurons with microvilli to the lateral olfactory tract indicates their participation in feeding behaviour in crucian carp. Chem. Senses 2001 , 26,  1139.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[27]   Sorensen P. W., Caprio J., Chemoreception, in The Physiology of Fishes, 2nd edn 1998, pp. 375–406 (CRC Press: Boca Raton, FL).

[28]   K. B. Døving , R. Selset , G. Thommesen , Olfactory sensitivity to bile acids in salmonid fishes. Acta Physiol. Scand. 1980 , 108,  123.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[29]   L. S. Demski , J. G. Dulka , Functional-anatomical studies on sperm release evoked by electrical stimulation of the olfactory tract in goldfish. Brain Res. 1984 , 291,  241.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[30]   N. E. Stacey , A. L. Kyle , Effects of olfactory tract lesions on sexual and feeding behavior in the goldfish. Physiol. Behav. 1983 , 30,  621.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[31]   E. H. Hamdani , K. B. Døving , Specific projection of the sensory crypt cells in the olfactory system in crucian carp, Carassius carassius. Chem. Senses 2005 , 31,  63.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[32]   G. Thommesen , The spatial distribution of odour induced potentials in the olfactory bulb of char and trout (Salmonidae). Acta Physiol. Scand. 1978 , 102,  205.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[33]   A. P. Scott , P. W. Sorensen , Time course of release of pheromonally active gonadal steroids and their conjugates by ovulatory goldfish. Gen. Comp. Endocrinol. 1994 , 96,  309.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[34]   E.-H. Hamdani , O. B. Stabell , G. Alexander , K. B. Døving , Alarm reaction in the crucian carp is mediated by the medial bundle of the medial olfactory tract. Chem. Senses 2000 , 25,  103.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[35]   R. M. Mesquita , A. V. Canario , E. Melo , Partition of fish pheromones between water and aggregates of humic acids. Consequences for sexual signaling. Environ. Sci. Technol. 2003 , 37,  742.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[36]   K. Matsumura , Tetrodotoxin as a pheromone. Nature 1995 , 378,  563.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[37]   W. Pfeiffer , G. Riegelbauer , G. Meier , B. Scheibler , Effect of hypoxanthine-3(N)-oxide and hypoxanthine-1(N)-oxide on central nervous excitation of the black tetra Gymnocorymbus ternetzi (Characidae, Ostariophysi, Pisces) indicated by dorsal light response. J. Chem. Ecol. 1985 , 11,  507.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[38]   P. W. Sorensen , T. J. Hara , N. E. Stacey , J. G. Dulka , Extreme olfactory specificity of male goldfish to the preovulatory steroidal pheromone 17α,20β-dihydroxy-4-pregnen-3-one. J. Comp. Physiol. A 1990 , 166,  373.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[39]   P. W. Sorensen , T. J. Hara , N. E. Stacey , F. W. Goetz , F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol. Reprod. 1988 , 39,  1039.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[40]   C. N. Polkinghorne , J. M. Olson , D. G. Gallaher , P. W. Sorensen , Larval sea lamprey release two unique bile acids** to the water at a rate sufficient to produce detectable riverine pheromone plumes. Fish Physiol. Biochem. 2001 , 24,  15.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[41]   K. Kawabata , Induction of sexual behavior in male fish (Rhodeus ocellatus ocellatus) by amino acids. Amino Acids 1993 , 5,  323.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[42]   J. Krieger , H. Breer , Olfactory reception in invertebrates. Science 1999 , 286,  720.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[43]   B. H. Sandler , L. Nikonova , W. S. Leal , J. Clardy , Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. Chem. Biol. 2000 , 7,  143.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[44]   A. L. Il’ichev , D. G. Williams , L. J. Gut , Dual pheromone dispenser for combined control of codling moth Cydia pomonella L. and oriental fruit moth Grapholita molesta (Busck) (Lep., Tortricidae) in pears. J. Appl. Entomol. 2007 , 131,  368.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[45]   P. W. Sorensen , L. A. Vrieze , The chemical ecology and potential application of the sea lamprey migratory pheromone. J. Great Lakes Res. 2003 , 29,  66.
         open url image1

[46]   W. Li , P. W. Sorensen , Highly independent olfactory receptor sites for naturally occurring bile acids in the sea lamprey, Petromyzon marinus. J. Comp. Physiol. A 1997 , 180,  429.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[47]   J. Fine , P. Sorensen , Isolation and biological activity of the multi-component sea lamprey migratory pheromone. J. Chem. Ecol. 2008 , 34,  1259.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[48]   W. Li , P. W. Sorensen , D. D. Gallaher , The olfactory system of migratory adult sea lamprey (Petromyzon marinus) is specifically and acutely sensitive to unique bile acids released by conspecific larvae. J. Gen. Physiol. 1995 , 105,  569.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[49]   P. W. Sorensen , L. A. Vrieze , J. M. Fine , A multi-component migratory pheromone in the sea lamprey. Fish Physiol. Biochem. 2003 , 28,  253.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[50]   P. W. Sorensen , T. R. Hoye , A critical review of the discovery and application of a migratory pheromone in an invasive fish, the sea lamprey Petromyzon marinus L. J. Fish Biol. 2007 , 71,  100.
         open url image1

[51]   P. W. Sorensen , J. M. Fine , V. Dvornikovs , C. S. Jeffrey , F. Shao , J. Wang , L. A. Vrieze , K. R. Anderson , T. R. Hoye , Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nat. Chem. Biol. 2005 , 1,  324.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[52]   T. R. Hoye , P. W. Sorensen , A critical review of the discovery and application of a migratory pheromone in an invasive fish, the sea lamprey Petromyzon marinus L. J. Fish Biol. 2007 , 71,  100.
         open url image1

[53]   M. C. Wagner , M. L. Jones , M. B. Twohey , P. W. Sorensen , A field test verifies that pheromones can be useful for sea lamprey (Petromyzon marinus) control in the Great Lakes. Can. J. Fish. Aquat. Sci. 2006 , 63,  475.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[54]   J. Brechbuhl , M. Klaey , M.-C. Broillet , Grueneberg ganglion cells mediate alarm pheromone detection in mice. Science 2008 , 321,  1092.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[55]   M. Hagman , R. Shine , Understanding the toad code: behavioural responses of cane toad (Chaunus marinus) larvae and metamorphs to chemical cues. Austral Ecol. 2008 , 33,  37.
         open url image1

[56]   J. Rajchard , Antipredator pheromones in amphibians: a review. Vet. Med. (Praha) 2006 , 51,  409.
         open url image1

[57]   E. G. Schwartzberg , G. Kunert , C. Stephan , A. David , U. S. R. Röse , J. Gershenzon , W. W. Weisser , Alarm pheromone emission by pea aphid, Acyrthosiphon pisum, clones under predation by lacewing larvae. Entomol. Exp. Appl. 2008 , 128,  403.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[58]   G. Kunert , S. Otto , U. S. R. Röse , J. Gershenzon , W. W. Weisse , Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecol. Lett. 2005 , 8,  596.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[59]   M. Ono , H. Terabe , H. Hori , M. Sasaki , Components of giant hornet alarm pheromone. Nature 2003 , 424,  637.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[60]   A. R. Wardle , J. H. Borden , H. D. Pierce , R. Gries , Volatile compounds released by disturbed and calm adults of the tarnished plant bug, Lygus lineolaris. J. Chem. Ecol. 2003 , 29,  931.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[61]   G. E. Brown , J. C. Adrian , N. T. Naderi , M. C. Harvey , J. M. Kelly , Nitrogen oxides elicit antipredator responses in juvenile channel catfish, but not in convict cichlids or rainbow trout: conservation of the ostariophysan alarm pheromone. J. Chem. Ecol. 2003 , 29,  1781.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[62]   S. Lastein , E. H. Hamdani , K. B. Døving , Single unit responses to skin odorants from conspecifics and heterospecifics in the olfactory bulb of crucian carp Carassius carassius. J. Exp. Biol. 2008 , 211,  3529.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[63]   O. B. Stabeil , M. S. Lwin , Predator-induced phenotypic changes in crucian carp are caused by chemical signals from conspecifics. Environ. Biol. Fishes 1997 , 49,  145.
         open url image1

[64]   B. D. Wisenden , T. A. Thiel , Field verification of predator attraction to minnow alarm substance. J. Chem. Ecol. 2002 , 28,  433.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[65]   D. P. Chivers , G. E. Brown , R. J. F. Smith , The evolution of chemical alarm signals: Attracting predators benefits alarm signal senders. Am. Nat. 1996 , 148,  649.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[66]   S. Lastein , E. Höglund , I. Mayer , Ø. Øverli , K. B. Døving , Female crucian carp, Carassius carassius, lose predator avoidance behavior when getting ready to mate. J. Chem. Ecol. 2008 , 34,  1487.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[67]   Carr W. E. S., The role of the chemical senses and specific chemicals in controlling different facets of the behavior of aquatic animals, in From Structure to Information in Sensory Systems 1996, pp. 3–24 (World Scientific: Italy).

[68]   P. W. Sørensen , A. P. Scott , The evolution of hormonal sex pheromones in teleost fish: poor correlation between the pattern of steroid release by goldfish and olfactory sensitivity suggests that these cues evolved as a result of chemical spying rather than signal specialization. Acta Physiol. Scand. 1994 , 152,  191.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[69]   Stacey N. E., Cardwell J. R., Liley N. R., Scott A. P., Sorensen P. W., Hormones as sex pheromones in fish, in Perspectives in Comparative Endocrinology (Eds K. G. Davey, R. E. Peter, S. Tobe) 1994, pp. 438–448 (National Research Council of Canada).

[70]   P. W. Sorensen , T. A. Christensen , N. E. Stacey , Discrimination of pheromonal cues in fish: emerging parallels with insects. Curr. Opin. Neurobiol. 1998 , 8,  458.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[71]   F. Yamazaki , The role of urine in sex discrimination in the goldfish Carassius auratus. Bull. Fac. Fish. Hokkaido Univ. 1990 , 41,  155.
         open url image1

[72]   J. S. Richards , D. L. Russell , S. Ochsner , M. Hsieh , K. H. Doyle , A. E. Falender , Y. K. Lo , S. C. Sharma , Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog. Horm. Res. 2002 , 57,  195.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[73]   D. R. Kelly , When is a butterfly like an elephant? Chem. Biol. 1996 , 3,  595.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[74]   K. R. Poling , E. J. Fraser , P. W. Sorensen , The three steroidal components of the goldfish preovulatory pheromone signal evoke different behaviors in males. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2001 , 129,  645.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[75]   A. N. C. Morse , D. E. Morse , Recruitment and metamorphosis of Haliotis larvae induced by molecules uniquely available at the surfaces of crustose red algae. J. Exp. Mar. Biol. Ecol. 1984 , 75,  191.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[76]   R. A. Jensen , D. E. Morse , Chemically induced metamorphosis of polychaete larvae in both the laboratory and ocean environment. J. Chem. Ecol. 1990 , 16,  911.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[77]   J. Kubanek , M. E. Hay , P. J. Brown , N. Lindquist , W. Fenical , Lignoid chemical defenses in the freshwater macrophyte Saururus cernuus. Chemoecology 2001 , 11,  1.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[78]   S. A. Miller , F. D. Provenza , Mechanisms of resistance of freshwater macrophytes to herbivory by invasive juvenile common carp. Freshw. Biol. 2007 , 52,  39.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[79]   J. E. Murphy , K. B. Beckmen , J. K. Johnson , R. B. Cope , T. Lawmaster , V. R. Beasley , Toxic and feeding deterrent effects of native aquatic macrophytes on exotic grass carp (Ctenopharyngodon idella). Ecotoxicology 2002 , 11,  243.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[80]   J. Parker , D. Collins , J. Kubanek , M. Sullards , D. Bostwick , M. Hay , Chemical defenses promote persistence of the aquatic plant Micranthemum umbrosum. J. Chem. Ecol. 2006 , 32,  815.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[81]   D. M. Wilson , W. Fenical , M. Hay , N. Lindquist , R. Bolser , Habenariol, a freshwater feeding deterrent from the aquatic orchid Habenaria repens (Orchidaceae). Phytochemistry 1999 , 50,  1333.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[82]   Norris J. N., Fenical W., Chemical defence in tropical marine algae, in The Atlantic Barrier Reef Ecosystem at Carrie Bow Bay, Belize. I. Structure and Communities 1982, pp. 417–431 (Smithsonian Institution Press: Washington, DC).

[83]   C. D. Runcie , Behavioral evidence for multicomponent trail pheromone in the termite, Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae). J. Chem. Ecol. 1987 , 13,  1967.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[84]   H. D. Bloom , A. Perlmutter , A sexual aggregating pheromone system in the zebrafish, Brachydanio rerio (hamilton-buchanan). J. Exp. Zool. 1977 , 199,  215.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[85]   D. Park , C. R. Propper , Pheromones from female mosquitofish at different stages of reproduction differentially affect male sexual activity. Copeia 2002 , 2002,  1113.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[86]   K. Mopper , A. Stubbins , J. D. Ritchie , H. M. Bialk , P. G. Hatcher , Advanced instrumental approaches for characterization of marine dissolved organic matter: extraction techniques, mass spectrometry, and nuclear magnetic resonance spectroscopy. Chem. Rev. 2007 , 107,  419.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[87]   A. V. Jung , C. Frochot , S. Parant , B. S. Lartiges , C. Selve , M. L. Viriot , J.-L. Bersillon , Synthesis of amino-phenolic humic-like substances and comparison with natural aquatic humic acids: A multi-analytical techniques approach. Org. Geochem. 2005 , 36,  1252.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[88]   H. Zenkevics , M. Klavins , V. Vose , A. Bucena , Humic acid reduces gonadotropin activity and hormonal sensitivity of frog oocytes. Aquat. Toxicol. 2005 , 75,  380.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[89]   R. Menzel , S. Sturzenbaum , A. Barenwaldt , J. Kulas , C. E. Steinberg , Humic material induces behavioral and global transcriptional responses in the nematode Caenorhabditis elegans. Environ. Sci. Technol. 2005 , 39,  8324.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[90]   S. J. Cooke , R. S. McKinley , Winter residency and activity patterns of channel catfish, Ictalurus punctatus (Rafinesque), and common carp, Cyprinus carpio L., in a thermal discharge canal. Fish. Manag. Ecol. 1999 , 6,  515.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[91]   C. Tseng , L. Liu , C. Chen , W. Ding , Analysis of perfluorooctanesulfonate and related fluorochemicals in water and biological tissue samples by liquid chromatography-ion trap mass spectrometry. J. Chromatogr. A 2006 , 1105,  119.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[92]   L. E. Hurd , F. R. Prete , T. H. Jones , T. B. Singh , J. E. Co , R. T. Portman , First identification of a putative sex pheromone in a praying mantis. J. Chem. Ecol. 2004 , 30,  155.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[93]   M. N. Kayali-Sayadi , J. M. Bautista , L. M. Polo-Díez , I. Salazar , Identification of pheromones in mouse urine by head-space solid phase microextraction followed by gas chromatography-mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2003 , 796,  55.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[94]   A. L. Il’ichev , L. L. Stelinski , D. G. Williams , L. J. Gut , Sprayable microencapsulated sex pheromone formulation for mating disruption of oriental fruit Moth (Lepidoptera: Tortricidae) in Australian peach and pear orchards. J. Econ. Entomol. 2006 , 99,  2048.
        | PubMed |  open url image1