Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Grass carp (Ctenopharyngodon idella) translocations, including hitchhiker introductions, alter zooplankton communities in receiving ponds

Suzanne N. Branford A and Ian C. Duggan A B
+ Author Affiliations
- Author Affiliations

A Environmental Research Institute, School of Science, The University of Waikato, Private Bag 3015, Hamilton 3240, New Zealand.

B Corresponding author. Email: i.duggan@waikato.ac.nz

Marine and Freshwater Research 68(12) 2216-2227 https://doi.org/10.1071/MF17051
Submitted: 24 February 2017  Accepted: 20 April 2017   Published: 29 June 2017

Abstract

In the present study we tested the effects of translocations from aquaculture facilities of grass carp, one of the most commonly used species in aquaculture globally, to constructed ponds in the Auckland region, New Zealand. Primarily, we were interested in whether zooplankton assemblages in recipient ponds are affected by the concomitant introduction of ‘hitchhikers’ with fish releases. Zooplankton community composition was quantified in 34 ponds that had been subject to grass carp release and 31 that had no grass carp introductions. A significant difference in zooplankton community composition was observed between ponds that had received grass carp translocations and those that had not. Differences in community composition between ponds with and without carp releases could be attributed to both the: (1) effects of activity of grass carp through habitat modification; and (2) establishment of hitchhiking zooplankton species originating from aquaculture ponds, including non-native species. Effective measures to curb the proliferation of non-native taxa within aquaculture facilities, and to mitigate the accidental movement of non-native taxa with translocations from these facilities, are required to reduce future zooplankton introductions.

Additional keywords: aquaculture, calanoid copepods, Daphnia pulex, exotic species, invasion vectors, Skistodiaptomus pallidus.


References

Alfonso, G., and Belmonte, G. (2008). Expanding distribution of Boeckella triarticulata (Thomson, 1883) (Copepoda: Calanoida: Centropagidae) in Southern Italy. Aquatic Invasions 3, 247–251.
Expanding distribution of Boeckella triarticulata (Thomson, 1883) (Copepoda: Calanoida: Centropagidae) in Southern Italy.Crossref | GoogleScholarGoogle Scholar |

Balvert, S. F., Duggan, I. C., and Hogg, I. D. (2009). Zooplankton seasonal dynamics in a recently filled mine pit lake: the effect of non-indigenous Daphnia establishment. Aquatic Ecology 43, 403–413.
Zooplankton seasonal dynamics in a recently filled mine pit lake: the effect of non-indigenous Daphnia establishment.Crossref | GoogleScholarGoogle Scholar |

Banks, C. M., and Duggan, I. C. (2009). Lake construction has facilitated calanoid copepod invasions in New Zealand. Diversity & Distributions 15, 80–87.
Lake construction has facilitated calanoid copepod invasions in New Zealand.Crossref | GoogleScholarGoogle Scholar |

Bartley, D. M. (2011). Aquaculture. In ‘Encyclopedia of Biological Invasions’. (Eds D. Simberloff and M Rejmanek.) pp. 27–32. (University of California Press: Oakland, CA, USA.)

Bayly, I. A. E. (1967). New species of Boeckella (Copepoda: Calanoida) and additional comments on some other species of the genus. Papers and Proceedings of the Royal Society of Tasmania 101, 97–102.

Bayly, I. A. E. (1992). ‘Non-Marine Centropagidae (Copepoda: Calanoida) of the World. Guides to the Identification of the Microinvertebrates of the Continental Waters of the World 2.’ (SPB Academic Publishing: The Hague, Netherlands.)

Belal, I. E. H. (2007). Controlling aquatic weeds in a Saudi drainage canal using grass carp (Ctenopharyngodon idella Val.). Journal of Food Agriculture and Environment 5, 332–336.

Bostock, J., McAndrew, B., Richards, R., Jauncey, K., Telfer, T., Lorenzen, K., Little, D., Ross, L., Handisyde, N., Gatward, I., and Corner, R. (2010). Aquaculture: global status and trends. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365, 2897–2912.
Aquaculture: global status and trends.Crossref | GoogleScholarGoogle Scholar |

Burns, C. W. (2013). Predictors of invasion success by Daphnia species: influence of food, temperature and species identity. Biological Invasions 15, 859–869.
Predictors of invasion success by Daphnia species: influence of food, temperature and species identity.Crossref | GoogleScholarGoogle Scholar |

Burns, N. M., Rutherford, J. C., and Clayton, J. S. (1999). A monitoring and classification system for New Zealand lakes and reservoirs. Lake and Reservoir Management 15, 255–271.
A monitoring and classification system for New Zealand lakes and reservoirs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvFOns7k%3D&md5=7098bd983749f11604d98b96b22d2745CAS |

Byron, E. R., and Saunders, J. F. (1981). Colonization of Lake Tahoe and other western habitats by the copepod, Skistodiaptomus pallidus (Herrick) (Calanoida). The Southwestern Naturalist 26, 82–83.
Colonization of Lake Tahoe and other western habitats by the copepod, Skistodiaptomus pallidus (Herrick) (Calanoida).Crossref | GoogleScholarGoogle Scholar |

Chapman, M. A., and Green, J. D. (1987). Zooplankton ecology. In ‘Inland Waters of New Zealand’. (Ed A. B. Viner.) DSIR bulletin 241, pp. 225–263. (Department of Scientific and Industrial Research: Wellington, New Zealand.)

Chapman, M. A., Lewis, M. H., and Winterbourn, M. J. (2011). ‘Guide to the Freshwater Crustacea of New Zealand.’ (New Zealand Freshwater Sciences Society: Christchurch, New Zealand.)

Clarke, K. R., and Warwick, R. M. (1994). ‘Change in Marine Communities: an Approach to Statistical Analysis and Interpretation’, 2nd edn. (Plymouth Marine Laboratory, National Research Council: Plymouth, UK.)

Dall Armellina, A. A., Bezic, C. R., and Gajardo, O. A. (1999). Submerged macrophyte control with herbivorous fish in irrigation channels of semiarid Argentina. Hydrobiologia 415, 265–269.
Submerged macrophyte control with herbivorous fish in irrigation channels of semiarid Argentina.Crossref | GoogleScholarGoogle Scholar |

Don, G. L. (2015). Rosedale wastewater treatment plant – treatment pond avifauna November 2014 to June 2015. Prepared for Watercare Services Ltd. Bioresearches Group Ltd, Auckland, New Zealand.

Duggan, I. C. (2007). ‘An Assessment of the Water Quality of Ten Waikato Lakes Based on Zooplankton Community Composition’. (Environment Waikato: Hamilton, New Zealand.)

Duggan, I. C., and Pullan, S. (2017). Do freshwater aquaculture facilities provide an invasion risk for zooplankton hitchhikers? Biological Invasions 19, 307–314.
Do freshwater aquaculture facilities provide an invasion risk for zooplankton hitchhikers?Crossref | GoogleScholarGoogle Scholar |

Duggan, I. C., Green, J. D., and Shiel, R. J. (2002). Distribution of rotifer assemblages in North Island, New Zealand, lakes: relationships to environmental and historical factors. Freshwater Biology 47, 195–206.
Distribution of rotifer assemblages in North Island, New Zealand, lakes: relationships to environmental and historical factors.Crossref | GoogleScholarGoogle Scholar |

Duggan, I. C., Green, J. D., and Burger, D. F. (2006). First New Zealand records of three non-indigenous zooplankton species: Skistodiaptomus pallidus, Sinodiaptomus valkanovi, and Daphnia dentifera. New Zealand Journal of Marine and Freshwater Research 40, 561–569.
First New Zealand records of three non-indigenous zooplankton species: Skistodiaptomus pallidus, Sinodiaptomus valkanovi, and Daphnia dentifera.Crossref | GoogleScholarGoogle Scholar |

Duggan, I. C., Robinson, K. V., Burns, C. W., Banks, J. C., and Hogg, I. D. (2012). Identifying invertebrate invasions using morphological and molecular analyses: North American Daphniapulex’ in New Zealand fresh waters. Aquatic Invasions 7, 585–590.
Identifying invertebrate invasions using morphological and molecular analyses: North American Daphniapulex’ in New Zealand fresh waters.Crossref | GoogleScholarGoogle Scholar |

Duggan, I. C., Neale, M. W., Robinson, K. V., Verburg, P., and Watson, N. T. N. (2014). Skistodiaptomus pallidus (Copepoda: Diaptomidae) establishment in New Zealand natural lakes, and its effects on zooplankton community composition. Aquatic Invasions 9, 195–202.
Skistodiaptomus pallidus (Copepoda: Diaptomidae) establishment in New Zealand natural lakes, and its effects on zooplankton community composition.Crossref | GoogleScholarGoogle Scholar |

Engel, K., Schreder, T., and Tollrian, R. (2014). Morphological defences of invasive Daphnia lumholtzi protect against vertebrate and invertebrate predators. Journal of Plankton Research 36, 1140–1145.
Morphological defences of invasive Daphnia lumholtzi protect against vertebrate and invertebrate predators.Crossref | GoogleScholarGoogle Scholar |

Ferrari, I., and Rossetti, G. (2006). New records of the centropagid Boeckella triarticulata (Thomson 1883) (Copepoda: Calanoida) in Northern Italy: evidence of a successful invasion. Aquatic Invasions 1, 219–222.
New records of the centropagid Boeckella triarticulata (Thomson 1883) (Copepoda: Calanoida) in Northern Italy: evidence of a successful invasion.Crossref | GoogleScholarGoogle Scholar |

Ferrari, I., Farabegoli, A., Pugnetti, A., and Stella, E. (1991). The occurrence of a calanoid Australasian species, Boeckella triarticulata (Thomson 1883), in fish ponds of Northern Italy. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 24, 2822–2827.

Fry, D. L., and Osborne, J. A. (1980). Zooplankton abundance and diversity in central Florida grass carp ponds. Hydrobiologia 68, 145–155.
Zooplankton abundance and diversity in central Florida grass carp ponds.Crossref | GoogleScholarGoogle Scholar |

Fuller, P. L., Nico, L. G., and Williams, J. D. (1999). Non-indigenous fishes introduced into inland waters of the United States. Special Publication 27. American Fisheries Society, Bethesda, MD, USA.

Gilbert, J. J. (1989). The effect of Daphnia interference on a natural rotifer and ciliate community: short-term bottle experiments. Limnology and Oceanography 34, 606–617.
The effect of Daphnia interference on a natural rotifer and ciliate community: short-term bottle experiments.Crossref | GoogleScholarGoogle Scholar |

Green, A. J., and Figuerola, J. (2005). Recent advances in the study of long‐distance dispersal of aquatic invertebrates via birds. Diversity & Distributions 11, 149–156.
Recent advances in the study of long‐distance dispersal of aquatic invertebrates via birds.Crossref | GoogleScholarGoogle Scholar |

Grosholz, E. D., Crafton, R. E., Fontana, R. E., Pasari, J. R., Williams, S. L., and Zabin, C. J. (2015). Aquaculture as a vector for marine invasions in California. Biological Invasions 17, 1471–1484.
Aquaculture as a vector for marine invasions in California.Crossref | GoogleScholarGoogle Scholar |

Hall, D. J., Threlkeld, S. T., Burns, C. W., and Crowley, P. H. (1976). The size–efficiency hypothesis and the size structure of zooplankton communities. Annual Review of Ecology and Systematics 7, 177–208.
The size–efficiency hypothesis and the size structure of zooplankton communities.Crossref | GoogleScholarGoogle Scholar |

Havel, J. E., and Hebert, P. D. N. (1993). Daphnia lumholtzi in North-America – another exotic zooplankter. Limnology and Oceanography 38, 1823–1827.
Daphnia lumholtzi in North-America – another exotic zooplankter.Crossref | GoogleScholarGoogle Scholar |

Havel, J. E., Lee, C. E., and Vander Zanden, M. J. (2005). Do reservoirs facilitate invasions into landscapes? Bioscience 55, 518–525.
Do reservoirs facilitate invasions into landscapes?Crossref | GoogleScholarGoogle Scholar |

He, S., Liang, X.-F., Li, L., Sun, J., and Shen, D. (2013). Differential gut growth, gene expression and digestive enzyme activities in young grass carp (Ctenopharyngodon idella) fed with plant and animal diets. Aquaculture 410–411, 18–24.
Differential gut growth, gene expression and digestive enzyme activities in young grass carp (Ctenopharyngodon idella) fed with plant and animal diets.Crossref | GoogleScholarGoogle Scholar |

Henry, M. (1924). Entomostraca collected in the vicinity of Auckland, New Zealand. Proceedings of the Linnean Society of New South Wales 49, 313–318.

Hofstra, D. E. (2014). Grass carp effectiveness and effects – stage 2: knowledge review. Prepared for the Department of Conservation. National Institute of Water and Atmospheric Research, Hamilton, New Zealand.

Hofstra, D. E., Rowe, D. K., and Clayton, J. S. (2014). Assessment of grass carp use for aquatic weed control: environmental impacts, management constraints and biosecurity risks in New Zealand waters. National Institute of Water and Atmospheric Research, Hamilton, New Zealand.

Hutchinson, G. E. (1967). ‘A Treatise on Limnology, Vol. II. Introduction to Lake Biology and the Limnoplankton.’ (Wiley: New York, NY, USA.)

June-Wells, M., Simpkins, T., Coleman, A. M., Henley, W., Jacobs, R., Aarrestad, P., Buck, G., Stevens, C., and Benson, G. (2017). Seventeen years of grass carp: an examination of vegetation management and collateral impacts in Ball Pond, New Fairfield, Connecticut. Lake and Reservoir Management 33, 84–100.
Seventeen years of grass carp: an examination of vegetation management and collateral impacts in Ball Pond, New Fairfield, Connecticut.Crossref | GoogleScholarGoogle Scholar |

Kirkagac, M., and Demir, N. (2004). The effects of grass carp on aquatic plants, plankton and benthos in ponds. Journal of Aquatic Plant Management 42, 32–39.

Koste, W. (1978). ‘Rotatoria, Die Rädertiere Mitteleuropas: Überordnung Monogononta.’ (Gebrüder Borntraeger: Berlin, West Germany.)

Kotov, A. A., and Taylor, D. J. (2014). Daphnia lumholtzi Sars, 1885 (Cladocera: Daphniidae) invades Argentina. Journal of Limnology 73, 369–374.
Daphnia lumholtzi Sars, 1885 (Cladocera: Daphniidae) invades Argentina.Crossref | GoogleScholarGoogle Scholar |

Lembi, C. A., Ritenour, B. G., Iverson, E. M., and Forss, E. C. (1978). Effects of vegetation removal by grass carp on water chemistry and phytoplankton in Indiana ponds. Transactions of the American Fisheries Society 107, 161–171.
Effects of vegetation removal by grass carp on water chemistry and phytoplankton in Indiana ponds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXkvFCkt7k%3D&md5=3416bcb200ff3b15fe16f14a18dd43a0CAS |

Maceina, M. J., Cichra, M. F., Betsill, R. K., and Bettoli, P. W. (1992). Limnological changes in a large reservoir following vegetation removal by grass carp. Journal of Freshwater Ecology 7, 81–95.
Limnological changes in a large reservoir following vegetation removal by grass carp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xis1Wqsbc%3D&md5=9ebf21339536e504ca18382405ef35e3CAS |

Maly, E., and Maly, M. (1997). Predation, competition, and co-occurrences of Boeckella and Calamoecia (Copepoda: Calanoida) in Western Australia. Hydrobiologia 354, 41–50.
Predation, competition, and co-occurrences of Boeckella and Calamoecia (Copepoda: Calanoida) in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Mitchell, C. P., Fish, G. R., and Burnet, A. M. R. (1984). Limnological changes in a small lake stocked with grass carp. New Zealand Journal of Marine and Freshwater Research 18, 103–114.
Limnological changes in a small lake stocked with grass carp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXotl2kuw%3D%3D&md5=c67ef3d5080834d320029250ffd9f8b6CAS |

Parkes, S. M., and Duggan, I. C. (2012). Are zooplankton invasions in constructed waters facilitated by simple communities? Diversity & Distributions 18, 1199–1210.
Are zooplankton invasions in constructed waters facilitated by simple communities?Crossref | GoogleScholarGoogle Scholar |

Pípalová, I. (2006). A review of grass carp use for aquatic weed control and its impact on water bodies. Journal of Aquatic Plant Management 44, 1–12.

Pípalová, I., Květ, J., and Adámek, Z. (2009). Limnological changes in a pond ecosystem caused by grass carp (Ctenopharyngodon idella Val.) low stocking density. Czech Journal of Animal Science 54, 31–45.

Rahel, F. J. (2007). Biogeographic barriers, connectivity and homogenization of freshwater faunas: it’s a small world after all. Freshwater Biology 52, 696–710.
Biogeographic barriers, connectivity and homogenization of freshwater faunas: it’s a small world after all.Crossref | GoogleScholarGoogle Scholar |

Richard, D. I., Small, J. W., and Osborne, J. A. (1985). Response of zooplankton to the reduction and elimination of submerged vegetation by grass carp and herbicide in four Florida lakes. Hydrobiologia 123, 97–108.
Response of zooplankton to the reduction and elimination of submerged vegetation by grass carp and herbicide in four Florida lakes.Crossref | GoogleScholarGoogle Scholar |

Segers, H. (2007). Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564, 1–104.

Shiel, R. J. (1995). ‘A Guide to Identification of Rotifers, Cladocerans and Copepods from Australian Inland Waters’. (Co-operative Research Centre for Freshwater Ecology: Albury, NSW, Australia.)

Shiel, R. J., Smales, L., Sterrer, W., Duggan, I. C., Pichelin, S., and Green, J. D. (2009). Phylum Gnathifera: lesser jaw worms, rotifers, thorny-headed worms. In ‘New Zealand Inventory of Biodiversity: Volume One. Kingdom Animalia – Radiata, Lophotrochozoa, Deuterostomia’. (Ed. D. P. Gordon.) pp. 137–158. (Canterbury University Press: Christchurch, New Zealand.)

Shurin, J. B. (2000). Dispersal limitation, invasion resistance, and the structure of pond zooplankton communities. Ecology 81, 3074–3086.
Dispersal limitation, invasion resistance, and the structure of pond zooplankton communities.Crossref | GoogleScholarGoogle Scholar |

Sorensen, K. H., and Sterner, R. W. (1992). Extreme cyclomorphosis in Daphnia lumholtzi. Freshwater Biology 28, 257–262.
Extreme cyclomorphosis in Daphnia lumholtzi.Crossref | GoogleScholarGoogle Scholar |

Strayer, D. L. (2010). Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshwater Biology 55, 152–174.
Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future.Crossref | GoogleScholarGoogle Scholar |

Strecker, A. L., and Arnott, S. E. (2008). Invasive predator, Bythotrephes, has varied effects on ecosystem function in freshwater lakes. Ecosystems 11, 490–503.
Invasive predator, Bythotrephes, has varied effects on ecosystem function in freshwater lakes.Crossref | GoogleScholarGoogle Scholar |

Taylor, C. A., and Duggan, I. C. (2012). Can biotic resistance be utilized to reduce establishment rates of non-indigenous species in constructed waters? Biological Invasions 14, 307–322.
Can biotic resistance be utilized to reduce establishment rates of non-indigenous species in constructed waters?Crossref | GoogleScholarGoogle Scholar |

Vanni, M. J. (1986). Competition in zooplankton communities: suppression of small species by Daphnia pulex. Limnology and Oceanography 31, 1039–1056.
Competition in zooplankton communities: suppression of small species by Daphnia pulex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXit12itw%3D%3D&md5=e9cb59fa96502ed6761f2829b5b1754cCAS |

Von Holle, B., and Simberloff, D. (2005). Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86, 3212–3218.
Ecological resistance to biological invasion overwhelmed by propagule pressure.Crossref | GoogleScholarGoogle Scholar |

Watkins, C. E., Shireman, J. V., Rottmann, R. W., and Colle, D. E. (1981). Food habits of fingerling grass carp. Progressive Fish-Culturist 43, 95–97.
Food habits of fingerling grass carp.Crossref | GoogleScholarGoogle Scholar |