CESTODES AND THE SUCCESS OF AN INVASION: The case of the American brine shrimp

1. * * Flamingolepis liguloides Flamingolepis flamingo Wardium stellorae Fimbriarioides tadornae Eurycestus avoceti Anomotaenia tringae Anomotaenia microphallos Gynandrotaeniasp. * * * * * * AF AS AF AS AF AS AF AS AF AS AF AS AF AS AF AS January P(%) 1.5 0.9 1.1 0.0 0.0 0.0 0.0 0.0 0.4 0.0 0.0 0.0 0.0 0.0 0.0 0.0 MI ( ±SE ) 1 . 00 ( ± 0 . 00 ) 1.00 1 . 00 ( ± 0 . 00 ) 0.00 0.00 0.00 0.00 0.00 1.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 MA ( ±SE ) 0 . 0150 ( ± 0 . 01 ) 0 . 8929 ( ± 0 . 01 ) 0 . 0113 ( ± 0 . 01 ) 0.00 0.00 0.00 0.00 0.00 0 . 0038 ( ± 0 . 00 ) 0.00 0.00 0.00 0.00 0.00 0.00 0.00 February P(%) 4.6 21.4 1.0 5.0 0.0 0.0 0.5 0.0 0.5 0.0 0.0 0.0 0.0 0.0 0.5 1.4 MI ( ±SE ) 1 . 00 ( ± 0 . 00 ) 1 . 07 ( ± 0 . 05 ) 1 . 00 ( ± 0 . 00 ) 1 . 14 ( ± 0 . 14 ) 0.00 0.00 1.00 0.00 1.00 0.00 0.00 0.00 0.00 0.00 1.00 1 . 00 ( ± 0 . 00 ) MA ( ±SE ) 0 . 0457 ( ± 0 . 01 ) 0 . 2286 ( ± 0 . 04 ) 0 . 0102 ( ± 0 . 01 ) 0 . 0571 ( ± 0 . 02 ) 0.00 0.00 0 . 0051 ( ± 0 . 01 ) 0.00 0 . 0051 ( ± 0 . 01 ) 0.00 0.00 0.00 0.00 0.00 0 . 0051 ( ± 0 . 01 ) 0 . 0143 ( ± 0 . 01 ) March P(%) 0.5 12.1 1.4 0.7 0.0 0.4 0.0 0.4 2.8 1.8 0.0 0.0 0.0 0.0 0.9 0.4 MI ( ±SE ) 1.00 1 . 09 ( ± 0 . 05 ) 1 . 00 ( ± 0 . 00 ) 1 . 00 ( ± 0 . 00 ) 0.00 1.00 0.00 1.00 1 . 00 ( ± 0 . 00 ) 1 . 00 ( ± 0 . 00 ) 0.00 0.00 0.00 0.00 1 . 00 ( ± 0 . 00 ) 1.00 MA ( ±SE ) 0 . 0047 ( ± 0 . 00 ) 0 . 1321 ( ± 0 . 02 ) 0 . 0140 ( ± 0 . 01 ) 0 . 0071 ( ± 0 . 01 ) 0.00 0 . 0036 ( ± 0 . 00 ) 0.00 0 . 0036 ( ± 0 . 00 ) 0 . 0279 ( ± 0 . 01 ) 0 . 0179 ( ± 0 . 01 ) 0.00 0.00 0.00 0.00 0 . 0093 ( ± 0 . 01 ) 0 . 0036 ( ± 0 . 00 ) April P(%) 0.0 8.2 0.3 1.02 0.0 0.0 0.0 0.0 0.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 MI ( ±SE ) 0.00 1 . 13 ( ± 0 . 09 ) 1.00 1 . 00 ( ± 0 . 01 ) 0.00 0.00 0.00 0.00 1.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 MA ( ±SE ) 0.00 0 . 0918 ( ± 0 . 02 ) 0 . 0031 ( ± 0 . 00 ) 0 . 0102 ( ± 0 . 01 ) 0.00 0.00 0.00 0.00 0 . 0031 ( ± 0 . 00 ) 0.00 0.00 0.00 0.00 0.00 0.00 0.00 May P(%) 0.4 50.6 7.4 3.9 2.9 3.9 3.7 0.0 15.7 14.3 10.7 44.2 1.7 0.0 0.4 0.0 MI ( ±SE ) 3.00 1 . 51 ( ± 0 . 15 ) 1 . 06 ( ± 0 . 06 ) 1 . 00 ( ± 0 . 00 ) 1 . 14 ( ± 0 . 14 ) 1 . 00 ( ± 0 . 00 ) 1 . 00 ( ± 0 . 00 ) 0.00 1 . 03 ( ± 0 . 03 ) 1 . 00 ( ± 0 . 00 ) 1 . 12 ( ± 0 . 08 ) 1 . 15 ( ± 0 . 07 ) 1 . 00 ( ± 0 . 00 ) 0.00 1.00 0.00 MA ( ±SE ) 0 . 0124 ( ± 0 . 01 ) 0 . 7662 ( ± 0 . 12 ) 0 . 0785 ( ± 0 . 02 ) 0 . 0390 ( ± 0 . 02 ) 0 . 0331 ( ± 0 . 01 ) 0 . 0390 ( ± 0 . 02 ) 0 . 0372 ( ± 0 . 01 ) 0.00 0 . 1612 ( ± 0 . 02 ) 0 . 1429 ( ± 0 . 04 ) 0 . 1198 ( ± 0 . 02 ) 0 . 5065 ( ± 0 . 07 ) 0 . 0165 ( ± 0 . 01 ) 0.00 0 . 0041 ( ± 0 . 00 ) 0.00 QUANTITATIVE DESCRIPTORS OF TOTAL INFECTION Artemia franciscana # 42 CESTODES AND THE SUCCESS OF AN INVASION: The case of the American brine shrimp Artemia franciscana in a Mediterranean saltern Stella REDÓN¹, N. Berthelemy-Okazaki²,B.B. Georgiev3,G.P. Vasileva3,P.N. Nikolov3,M. Maccari¹, F. Hontoria¹,F. Amat¹ 1 Instituto de Acuicultura de Torre de la Sal (CSIC), 12595 Ribera de Cabanes (Castellón), Spain. 2 Department of Zoology, College of Science. Weber State University, 2505 University Circle. Ogden UT 84408-2505, U.S.A. 3Central Laboratory of General Ecology. Bulgarian Academy of Sciences. 2 Gagarin Street,1113 Sofia, Bulgaria. Abstract The American brine shrimp Artemia franciscana became an invasive species in the Iberian Peninsula and in the Western Mediterranean salterns, where is eradicating native Artemia species (Amat et al., 2005; Amat et al., 2007). Brine shrimps act as intermediate hosts of several water bird cestodes (Cyclophyllidea). When invasive species leave their original range and escape from their coevolved parasites, they can experience a demographic release (Enemy Release hypothesis) in the new range, becoming highly competitive and threatening biodiversity there. The aim of this work was to assess whether the invasive A. franciscana is affected by avian cestode cysticercoids to the same extent as the native A. salina. The natural infection of both bisexual species was studied in La Trinitat salterns (Tarragona Province, Spain) from January until May when they cooccur. The additional purpose of this work was to afford the first data on the cestode parasitism found in A. franciscana in its native range (Great Salt Lake, Utah). The morphological identification of the cysticercoids was based on previous descriptions (Georgiev et al., 2005; Vasileva et al., 2009). In La Trinitat salterns, levels of overall infection are markedly lower in the invasive than in the native brine shrimp species. The prevalence ranged between 0.6 and 37.2 for A. franciscana and between 0.9 and 75.3 for A. salina. The mean intensity varied between 1 and 1.24 for the invasive species and between 1 and 1.98 for the native one. Flamingolepis liguloides, parasitizing flamingos, showed significantly higher prevalences and mean abundances in A. salina than in the American brine shrimp. Cysticercoids from mainly dilepidid species (mostly Eurycestus avoceti) were parasitizing the invasive A. franciscana. However, only Confluaria podicipina (parasitizing grebes) and Wardium spp. (parasitizing gulls) were recorded in the A. franciscana native range. Our results suggest that cestodes play an important role in the competitive interaction between native and alien brine shrimps and they could partially explain the A. franciscana invasion success. In the Mediterranean, Artemia species (Branchiopoda, Anostraca) are involved as intermediate hosts in the life cycles of several trophically transmitted helminth parasites, mainly cyclophillidean cestodes, of water birds. CESTODE SPECIES AND FINAL HOSTS SITE: La Trinitat salterns (40º34´58´´N, 00º40´49´´E) are located on the Mediterranean coast of Spain, in the Tarragona Province. It is one of the most important habitats for local and migrating birds. It is the only Mediterranean hypersaline ecosystem where both bisexual brine shrimp species are coocurring: A. salina(native) A. franciscana (alien invader) • HYMENOLEPIDIDAE • Flamingolepis liguloides (flamingos) • Flamingolepis flamingo (flamingos) • Confluaria podicipina (grebes) • Wardium stellorae (gulls) • Branchiopodataenia gvozdevi (Larus genei) • Fimbriarioides tadornae • (shelducks: Tadorna tadorna) • DILEPIDIDAE • Eurycestus avoceti (avocets, flamingos) • Anomotaenia tringae • (waders: Tringa and Calidris) • Anomotaenia microphallos • (waders: Tringa and Calidris) Artemia salina (males) • PROGYNOTAENIIDAE • Gynandrotaenia stammeri (flamingos) • Gynandrotaenia sp. (flamingos) Infected individuals • AIM: • To study the role that cestode parasites can play in the competitive interactions between two brine shrimp species, the exotic invasive Artemia franciscana and the native Artemia salina, in order to explain the invasion success of the American brine shrimp. • To afford a preliminary data on cestode parasites in A. franciscana in its native range (Great Salt Lake). ENEMY RELEASE HYPOTHESIS The success of an invader is related to a reduction in natural enemies (predators, parasites, etc.) in the new range in comparison with the native range (Keane and Crawley, 2002; Torchin et al., 2003). LA TRINITAT SALTERNS CESTODE PARASITE DIVERSITY INFECTION DESCRIPTORS: prevalence (P), mean intensity (MI) and mean abundance (MA). SE, standard error. Phoenicopterus ruber Infected A. salina • During the coexistence period of both brine shrimp species (January to May), levels of overall infection are significantly lower in the exotic invasive brine shrimp A. franciscana than in the native A. salina. • Eight cestode species were shared by both Artemia species. However, statistically significant differences were recorded in prevalences and mean abundances of cestodes parasitic in flamingos, especially F. liguloides, in alien versus indigenous shrimps. F. liguloides GREAT SALT LAKE MORPHOLOGICAL IDENTIFICATION OF CYSTICERCOIDS RELATIVE ABUNDANCE (RA%) OF CESTODE SPECIES Confluaria podicipina Wardium fusa ANTELOPE ISLAND ANTELOPE ISLAND CAUSEWAY • Eared grebes • Sea gulls • American avocets • Wilson´s Phalaropes • Red-necked Phalaropes • Black-necked stilts Unidentified cysticercoids SALTAIR MARINA Hymenolepidid Dilepidid rostellar hooks rostellar hooks • Cysticercoids of three cestode hymenolepidids and one dilepidid were recorded in A. franciscana in its native habitat. • Confluaria podicipina and Wardium fusa are the most abundant cestode species in GSL. Conclusions • The invasive A. franciscana appears to be resistant to several native cestode species (parasitic in flamingos) which have high prevalences in the native A. salina. • Cestodes infect at higher rates native Artemia species than the invasive A. franciscana so maybe influencing the outcome of their competitive interactions.ENEMY RELEASE may be a key factor in • the invasion success of A. franciscana. CESTODES PLAY AN IMPORTANT ROLE IN THE COMPETITIVE INTERACTION BETWEEN NATIVE AND ALIEN BRINE SHRIMPS AND THEY COULD PARTIALLY EXPLAIN THE A. franciscana INVASION SUCCESS IN THE WESTERN MEDITERRANEAN REGION. REFERENCES ACKNOWLEDGEMENTS AMAT, F., HONTORIA, F., RUIZ, O., GREEN, A.J., SANCHEZ, M.I., FIGUEROLA, J., and HORTAS, F., 2005. Biological Invasions 7: 37-47. AMAT, F., HONTORIA, F., NAVARRO, J.C., VIEIRA, N., and MURA, G., 2007 Limnetica 26:177-194. GEORGIEV, B.B., SÁNCHEZ, M.I., GREEN, A.J., NIKOLOV, P.N., VASILEVA, G.P. and MAVRODIEVA, R.S., 2005. Acta Parasitologica 50 (2): 105-117. KEANE, R.M. and CRAWLEY, M.J., 2002. Trends in Ecology and Evolution 17: 164-170. TORCHIN , M.E., LAFFERTY, K.D., DOBSON, A.P., Mc KENZIE, V.J., and KURIS, A.M., 2003. Nature 421: 628-630. VASILEVA, G.P., REDÓN S., AMAT, F., NIKOLOV, P.N., SÁNCHEZ, M.I., LENORMAND, T. and GEORGIEV, B.B. 2009. Acta Parasitologica 54 (2): 143-150. This study has been funded by the Spanish Ministry of Science and Innovation (project CGL2005-02306/BOS).