Abstract
The tropical ascidian Herdmania momus (Savigny 1816) has been rapidly expanding its distribution in the Eastern Mediterranean Basin. To examine the role of temperature resilience on its invasion success, we conducted monthly field surveys for two years at Achziv (Israel) Marine Protected Area, and examined the survival of adult individuals from native (Red Sea) and invasive (Mediterranean) populations under different temperature treatments. In addition, temperature effects on fertilization and larval development were examined in controlled laboratory conditions. Results indicate that temperature has a significant effect on H. momus from its early life stages through adulthood. Field surveys revealed a significant decline in H. momus abundance in the Mediterranean with the decrease in seawater temperature. Low temperature inhibited development of early life stages, and individuals from both populations demonstrated low survivability under low temperature treatment. All the above may be derived from the tropical origin of H. momus, and may further limit its dispersal into colder areas. However, adult individuals from the invasive population demonstrated significantly higher survivability to the high temperature treatment in comparison to the native population from the Red Sea. Larvae development, metamorphosis and settlement were enhanced and with higher rates of success under the high temperature conditions. The high-temperature adaptation of the Mediterranean population of H. momus from fertilization to adulthood may thus contribute to its expanding distribution in the Eastern Mediterranean.








Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Azzurro E, Moschella P, Maynou F (2011) Tracking signals of change in Mediterranean fish diversity based on local ecological knowledge. PLoS ONE 6(9):e24885
Batty RS, Blaxter JHS, Bone Q (1991) The effect of temperature on the swimming of a teleost (Clupea harengus) and an ascidian larva (Dendrodoa grossularia). Comp Biochem Physiol A 100:297–300
Bayne BL (1965) Growth and the delay of metamorphosis of the larvae of Mytilus edulis (L.). Ophelia 2:1–47
Belanger CL, Jablonski D, Roy K, Berke SK, Krug AZ, Valentine JW (2012) Global environmental predictors of benthic marine biogeographic structure. P Natl Acad Sci 109:14046–14051
Bitar G, Ocaña O, Ramos-Esplá AA (2007) Contribution of the Red Sea alien species to structuring some benthic biocenosis in the Lebanon coast (Eastern Mediterranean). Rapp Comm Int Mer Médit 38:437
Braby CE, Somero GN (2006) Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). J Exp Biol 209:2554–2566
Byrne M, Gonzalez-Bernat M, Doo S, Foo S, Soars N, Lamare M (2013) Effects of ocean warming and acidification on embryos and non-calcifying larvae of the invasive sea star Patiriella regularis. Mar Ecol Prog Ser 473:235–246
Çinar ME, Bilecenoglu M, Öztürk B, Can A (2006) New records of alien species on the Levantine coast of Turkey. Aquat Invasions 1:84–90
Crickenberger S, Walther K, Moran AL (2017) Lower thermal limits to larval development do not predict poleward range limits of the introduced tropical barnacle Megabalanus coccopoma. Invertebr Biol 136:37–49
de Madron XD, Guieu C, Sempere R, Conan P, Cossa D, D’Ortenzio F, Estournel C, Gazeau F, Rabouille C, Stemmann L, Bonnet S (2011) Marine ecosystems’ responses to climatic and anthropogenic forcings in the Mediterranean. Prog Oceanogr 91:97–166
Dijkstra JA, Westerman EL, Harris LG (2017) Elevated seasonal temperatures eliminate thermal barriers of reproduction of a dominant invasive species: A community state change for northern communities? Divers Distrib 23:1182–1192
Dudas SE, Dower JF (2006) Reproductive ecology and dispersal potential of varnish clam Nuttallia obscurata, a recent invader in the Northeast Pacific ocean. Mar Ecol Prog Ser 320:195–205
Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139
Evans J, Borg JA, Schembri PJ (2013) First record of Herdmania momus (Ascidiacea: Pyuridae) from the central Mediterranean Sea. Mar Biodivers Rec 6:1–4
Fangue NA, Hofmeister M, Schulte PM (2006) Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J Exp Biol 209:2859–2872
Fowler AE, Gerner NV, Sewell MA (2011) Temperature and salinity tolerances of stage 1 zoeae predict possible range expansion of an introduced portunid crab, Charybdis japonica, in New Zealand. Biol Invasions 13:691–699
Gewing M, Shenkar N (2017) Monitoring the magnitude of marine vessel infestation by non-indigenous ascidians in the Mediterranean. Mar Pollut Bull 121:52–59
Gewing M, Rothman S, Raijman Nagar L, Shenkar N (2014) Early stages of establishment of the non-indigenous ascidian Herdmania momus (Savigny 1816) in shallow and deep water environments on natural substrates in the Mediterranean Sea. Biol Invasions Rec 3:77–81
Harant H (1927) Rapport sur les Tuniciers. Par J Zool 22:365–373
Harant H (1939) Les Fonds de Pêche Près D’Alexandrie: Ascidiacea (cartes 1–5). Imprimerie Nationale, Boulac
Hebert PD, Muncaster BW, Mackie GL (1989) Ecological and genetic studies on Dreissena polymorpha (Pallas): a new mollusc in the Great Lakes. Can J Fish Aquat Sci 46:1587–1591
Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008) Five potential consequences of climate change for invasive species. Conserv Biol 22:534–543
Hilbish TJ, Brannock PM, Jones KR, Smith AB, Bullock BN, Wethey DS (2010) Historical changes in the distributions of invasive and endemic marine invertebrates are contrary to global warming predictions: the effects of decadal climate oscillations. J Biogeogr 37:423–431
Hopkin RS, Qari S, Bowler K, Hyde D, Cuculescu M (2006) Seasonal thermal tolerance in marine Crustacea. J Exp Mar Biol Ecol 331:74–81
Hulme PE (2017) Climate change and biological invasions: evidence, expectations, and response options. Biol Rev 92:1297–1313
Izquierdo Muñoz A, Díaz Valdés M, Ramos-Esplá AA (2009) Recent non-indigenous ascidians in the Mediterranean Sea. Aquat Invasions 4:59–64
Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457–481
Keough MJ, Raimondi PT (1995) Responses of settling invertebrate larvae to bioorganic films: effects of different types of films. J Exp Mar Biol Ecol 185:235–253
Lord JP, Calini JM, Whitlatch RB (2015) Influence of seawater temperature and shipping on the spread and establishment of marine fouling species. Mar Biol 162:2481–2492
Manoj Nair R, Appukuttan KK (2003) Effect of temperature on the development, growth, survival and settlement of green mussel Perna viridis (Linnaeus 1758). Aquac Res 34:1037–1045
Marshall DJ, Styan CA, Keough MJ (2000) Intraspecific co-variation between egg and body size affects fertilization kinetics of free-spawning marine invertebrates. Mar Ecol Prog Ser 195:305–309
McCormick MI, Molony BW (1995) Influence of water temperature during the larval stage on size, age and body condition of a tropical reef fish at settlement. Mar Ecol Prog Ser 118:59–68
Nehring S (1998) Establishment of thermophilic phytoplankton species in the north sea: biological indicators of climatic changes? ICES J Mar Sci 55:818–823
Nishikawa T (2002) Revision of the ascidian genus Herdmania (Urochordata: Ascidiacea) inhabiting Japanese waters. JSSZ 7:217–250
Nyamukondiwa C, Kleynhans E, Terblanche JS (2010) Phenotypic plasticity of thermal tolerance contributes to the invasion potential of Mediterranean fruit flies (Ceratitis capitata). Ecol Entomol 35:565–575
Olive PJW (1995) Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. J Therm Biol 20:79–90
Ordóñez V, Rius M, McQuaid CD, Pineda MC, Pascual M, Turon X (2013) Early biotic interactions among introduced and native benthic species reveal cryptic predation and shifts in larval behaviour. Mar Ecol Prog Ser 488:65–79
Pachauri RK, Allen MR, Barros VR, Broome J, Cramer W, Christ R, Church JA, Clarke L, Dahe Q, Dasgupta P, Dubash NK (2014) Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change , p 151. IPCC
Pechenik JA (1984) The relationship between temperature, growth rate, and duration of planktonic life for larvae of the gastropod Crepidula fornicata (L). J Exp Mar Biol Ecol 74:241–257
Peck LS, Morley SA, Richard J, Clark MS (2014) Acclimation and thermal tolerance in Antarctic marine ectotherms. J Exp Biol 217:16–22
Pérès JM (1958) Ascidies recoltées sur les côtes Méditerranéennes d’Israel. B Res Counc Israel B 7:143–150
Peters RL, Lovejoy TE (1992) Global warming and biological diversity. Yale University Press, New Haven
Pineda MC, McQuaid CD, Turon X, López-Legentil S, Ordóñez V, Rius M (2012) Tough adults, frail babies: an analysis of stress sensitivity across early life-history stages of widely introduced marine invertebrates. PLoS ONE 7:e46672
Polo A, Yufera M, Pascual E (1991) Effects of temperature on egg and larval development of Sparus aurata L. Aquaculture 92:367–375
R Core Team (2016) R: A language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing. http://www.R-project.org. Accessed 2 Sept 2018
Rahel FJ, Olden JD (2008) Assessing the effects of climate change on aquatic invasive species. Conserv Biol 22:521–533
Rilov G (2016) Multi-species collapses at the warm edge of a warming sea. Sci Rep 6:36897
Rius M, Shenkar N (2012) Ascidian introductions through the Suez canal: the case study of an Indo-Pacific species. Mar Pollut Bull 64:2060–2068
Rocha RM, Castellano GC, Freire CA (2017) Physiological tolerance as a tool to support invasion risk assessment of tropical ascidians. Mar Ecol Prog Ser 577:105–119
Shenkar N, Loya Y (2008a) The solitary ascidian Herdmania momus: native (Red Sea) versus non-indigenous (Mediterranean) populations. Biol Invasions 10:1431–1439
Shenkar N, Loya Y (2008b) Ecology and systematics of the ascidian fauna in the Gulf of Eilat (Aqaba). In: Por FD (ed) Aqaba-Eilat, the improbable Gulf. Environment, biodiversity and preservation. Magnes Press, Jerusalem, pp 197–237
Shenkar N, Loya Y (2009) Non-indigenous ascidians (Chordata: Tunicata) along the Mediterranean coast of Israel. Mar Biodivers Rec 2:1–7
Somero GN (2012) The physiology of global change: linking patterns to mechanisms. Annu Rev Mar Sci 4:39–61
Sorte CJ, Williams SL, Zerebecki RA (2010) Ocean warming increases threat of invasive species in a marine fouling community. Ecology 91:2198–2204
Sorte CJ, Ibáñez I, Blumenthal DM, Molinari NA, Miller LP, Grosholz ED, Diez JM, D’Antonio CM, Olden JD, Jones SJ, Dukes JS (2013) Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance. Ecol Lett 16:261–270
Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. P Natl A Sci 99:15497–15500
Svane I, Young CM (1991) Sensory structures in tadpole larvae of the ascidians Microcosmus exasperatus Heller and Herdmania momus (Savigny). Acta Zool Stockh 72:129–135
Tepolt CK, Somero GN (2014) Master of all trades: thermal acclimation and adaptation of cardiac function in a broadly distributed marine invasive species, the European green crab, Carcinus maenas. J Exp Biol 217:1129–1138
The Israel national monitoring program at the Gulf of Eilat: http://www.iui-eilat.ac.il/Research/NMPMeteoData.aspx. Accessed 18 Mar 2018
Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45
Verween A, Vincx M, Degraer S (2007) The effect of temperature and salinity on the survival of Mytilopsis leucophaeata larvae (Mollusca, Bivalvia): The search for environmental limits. J Exp Mar Biol Ecol 348:111–120
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395
Wieczorek SK, Todd CD (1997) Inhibition and facilitation of bryozoan and ascidian settlement by natural multi-species biofilms: effects of film age and the roles of active and passive larval attachment. Mar Biol 128:463–473
Yeh PJ, Price TD (2004) Adaptive phenotypic plasticity and the successful colonization of a novel environment. Am Nat 164:531–542
Zabin CJ, Altieri A (2007) A Hawaiian limpet facilitates recruitment of a competitively dominant invasive barnacle. Mar Ecol Prog Ser 337:175–185
Zerebecki RA, Sorte CJ (2011) Temperature tolerance and stress proteins as mechanisms of invasive species success. PLoS ONE 6:e14806
Zhan A, Briski E, Bock DG, Ghabooli S, MacIsaac HJ (2015) Ascidians as models for studying invasion success. Mar Biol 162:2449–2470
Acknowledgements
We deeply thank the two anonymous reviewers for their constructive suggestions and criticism that greatly improved the manuscript. We are grateful to M. Novosolov for her constructive comments and advice, and to N. Paz for editorial assistance. We thank the Israel Nature and Parks Authority for their technical assistance in the field. Funding was provided by The FP7 Marie Curie CIG grant number 321547 to NS, and by the Israel Science Foundation Grant Number 993/15 to NS, by a student fellowship from the Mediterranean Sea Research Center of Israel to MG, and by the Caroline von Humboldt award to NS.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gewing, MT., Goldstein, E., Buba, Y. et al. Temperature resilience facilitates invasion success of the solitary ascidian Herdmania momus. Biol Invasions 21, 349–361 (2019). https://doi.org/10.1007/s10530-018-1827-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-018-1827-8


