Skip to main content

Advertisement

Log in

Herbivore and predator pressure in tidepools along an intertidal gradient: no consumption refuge for invasive species!

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Non-indigenous species (NIS) can invade marine ecosystems worldwide not only because of higher growth rates and reproductive potential but also due to their ability to escape from native consumers either by defensive traits or by the colonization of spatial refuges. Spatial consumption refuges can be present in tidepools, especially in those from the high shore, with harsh environmental conditions. In order to test this hypothesis, we quantified consumer pressure on NIS in tidepools with different tidal elevations. We deployed tethering assays within 73 tidepools at 30° S (Chile) in 2021 using the following four bait types: two NIS (the green seaweed Codium fragile and the tunicate Ciona robusta) and two reference baits (blades of the kelp Lessonia and dried squid). The two reference baits as well as the two NIS were consumed across all tidepools. Thus, there was no tidal gradient in NIS consumption: higher tidepools did not offer a spatial refuge as native consumers can reach them and consume NIS. Possibly, on wave-exposed coasts, high shore tidepools are frequently splashed, mitigating harsh conditions, and, therefore, reducing the potential for spatial refuges from consumption. While both NIS were eaten by native consumers in tidepools, they are nevertheless successful invaders. Therefore, our results suggest that NIS can compensate for consumer losses in tidepools, which allows them to colonize tidepool systems even if these do not offer spatial refuges from consumption. Tidepools might represent a first invasion window for NIS to enter natural communities, potentially causing important effects on biodiversity of rocky intertidal habitats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Aguilera MA (2011) The functional roles of herbivores in the rocky intertidal systems in Chile: a review of food preferences and consumptive effects. Rev Chil Hist Nat 84:241–261. https://doi.org/10.4067/S0716-078X2011000200009

    Article  Google Scholar 

  • Aguilera MA, Navarrete SA (2012) Functional identity and functional structure change through succession in a rocky intertidal marine herbivore assemblage. Ecology 93:75–89

    Article  PubMed  Google Scholar 

  • Aguilera MA, Broitman BR, Thiel M (2014) Spatial variability in community composition on a granite breakwater versus natural rocky shores: lack of microhabitats suppresses intertidal biodiversity. Mar Pollut Bull 87:257–268

    Article  CAS  PubMed  Google Scholar 

  • Aguilera MA, Aburto JA, Bravo L et al (2019a) Chile: environmental status and future perspectives. In: Sheppard C (ed) World seas: an environmental evaluation, 2nd edn. Academic Press, New York, pp 673–702

    Chapter  Google Scholar 

  • Aguilera MA, Broitman B, Vásquez J, Camus P (2019b) Consumer-resource interactions on an environmental mosaic: the role of top-down and bottom-up forcing of ecological interactions along the rocky shores of the temperate South-Eastern Pacific. In: Hawkins S, Bohn K, Firth L, Williams GA (eds) Interactions in the marine benthos: global patterns and processes. Cambridge University Press, Cambridge, pp 307–332

    Chapter  Google Scholar 

  • Astudillo JC, Bravo M, Dumont CP, Thiel M (2009) Detached aquaculture buoys in the SE Pacific: potential dispersal vehicles for associated organisms. Aquat Biol 5:219–231

    Article  Google Scholar 

  • Astudillo O, Dewitte B, Mallet M et al (2019) Sensitivity of the near-shore oceanic circulation off central Chile to coastal wind profiles characteristics. J Geophys Res Oceans 124:4644–4676. https://doi.org/10.1029/2018JC014051

    Article  Google Scholar 

  • Beck M (1998) Comparison of the measurement and effects of habitat structure on gastropods in rocky intertidal and mangrove habitats. Mar Ecol Prog Ser 169:165–178. https://doi.org/10.3354/meps169165

    Article  Google Scholar 

  • Bennett BA, Griffiths CL (1984) Factors affecting the distribution, abundance and diversity of rock-pool fishes on the Cape Peninsula, South Africa. Afr Zool 19:97–104

    Google Scholar 

  • Bertness MD (1981) Predation, physical stress, and the organization of a tropical rocky intertidal hermit crab community. Ecology 62:411–425

    Article  Google Scholar 

  • Bertness MD, Leonard GH, Levine JM, Schmidt PR, Ingraham AO (1999) Testing the relative contribution of positive and negative interactions in rocky intertidal communities. Ecology 80:2711–2726

    Article  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Broitman B, Navarrete S, Smith F, Gaines S (2001) Geographic variation of southeastern Pacific intertidal communities. Mar Ecol Prog Ser 224:21–34. https://doi.org/10.3354/meps224021

    Article  Google Scholar 

  • Brunetti R, Gissi C, Pennati R et al (2015) Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis. J Zool Syst Evol Res 53:186–193

    Article  Google Scholar 

  • Butchart SHM, Walpole M, Collen B et al (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168. https://doi.org/10.1126/science.1187512

    Article  CAS  PubMed  Google Scholar 

  • Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasión. Oecologia 130:146–156

    Article  PubMed  Google Scholar 

  • Carver CE, Mallet AL, Vercaemer B (2006) Biological synopsis of the solitary tunicate Ciona intestinalis. Can Manuscr Rep Fish Aquat Sci 2746:55

    Google Scholar 

  • Castilla JC, Steinmiller DK, Pacheco CJ (1998) Quantifying wave exposure daily and hourly on the intertidal rocky shore of central Chile. Rev Chil Hist Nat 71:19–25

    Google Scholar 

  • Connell JH (1961) Effects of competition, predation by Thais lapillus, and other factors on natural populations of barnacle Balanus balanoides. Ecol Monogr 31:61–104

    Article  Google Scholar 

  • Contreras S, Castilla J (1987) Feeding behavior and morphological adaptations in two sympatric sea urchin species in central Chile. Mar Ecol Prog Ser 38:217–224. https://doi.org/10.3354/meps038217

    Article  Google Scholar 

  • Cox TE, Baumgartner E, Philippoff J, Boyle KS (2011) Spatial and vertical patterns in the tidepool fish assemblage on the island of O`ahu. Environ Biol Fish 90:329–342

    Article  Google Scholar 

  • Davidson TM, Grupe BM (2015) Habitat modification in tidepools by bioeroding sea urchins and implications for fine-scale community structure. Mar Ecol 36:185–194

    Article  Google Scholar 

  • Dekker R, Beukema JJ (2012) Long-term dynamics and productivity of a successful invader: the first three decades of the bivalve Ensis directus in the western Wadden Sea. J Sea Res 71:31–40

    Article  Google Scholar 

  • Dethier MN (1980) Tidepools as refuges: Predation and the limits of the harpacticoid copepod Tigriopus californicus (Baker). J Exp Mar Biol Ecol 42:99–111. https://doi.org/10.1016/0022-0981(80)90169-0

    Article  Google Scholar 

  • Dethier MN (1984) Disturbance and recovery in intertidal pools: maintenance of mosaic patterns. Ecol Monogr 54:99–118. https://doi.org/10.2307/1942457

    Article  Google Scholar 

  • Díaz-Astudillo M, Saldías GS, Letelier J, Riquelme-Bugueño R (2022) Spatial and interannual variability in the distribution of euphausiid life stages in the permanent upwelling system off northern Chile. ICES Mar Sci 79:61–75

    Article  Google Scholar 

  • Duffy JE, Ziegler SL, Campbell JE, Bippus PM, Lefcheck JS (2015) Squidpops: a simple tool to crowdsource a global map of marine predation intensity. PLoS One 10(11):e0142994. https://doi.org/10.1371/journal.pone.0142994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dumont CP, Gaymer CF, Thiel M (2011a) Predation contributes to invasion resistance of benthic communities against the non-indigenous tunicate Ciona intestinalis. Biol Invasions 13:2023–2034. https://doi.org/10.1007/s10530-011-0018-7

    Article  Google Scholar 

  • Dumont CP, Harris LG, Gaymer CF (2011b) Anthropogenic structures as a spatial refuge from predation for the invasive bryozoan Bugula neritina. Mar Ecol Prog Ser 427:95–103

    Article  Google Scholar 

  • Dybern BI (1965) The life cycle of Ciona intestinalis (L.) f. typica in relation to the environmental temperature. Oikos 16:109. https://doi.org/10.2307/3564870

    Article  Google Scholar 

  • Epelbaum A, Herborg LM, Therriault TW, Pearce CM (2009) Temperature and salinity effects on growth, survival, reproduction, and potential distribution of two non-indigenous botryllid ascidians in British Columbia. J Exp Mar Biol Ecol 369:43–52. https://doi.org/10.1016/j.jembe.2008.10.028

    Article  Google Scholar 

  • Forrest BM, Fletcher LA, Atalah J et al (2013) Predation limits spread of Didemnum vexillum into natural habitats from refuges on anthropogenic structures. PLoS One 8:e82229. https://doi.org/10.1371/journal.pone.0082229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox J, Monette G (1992) Generalized collinearity diagnostics. JASA 87:178–183

    Article  Google Scholar 

  • Gagnon K, McKindsey CW, Johnson LE (2011) Dispersal potential of invasive algae: the determinants of buoyancy in Codium fragile spp. fragile. Mar Biol 158:2449–2458

    Article  Google Scholar 

  • Gallardo B, Clavero M, Sánchez MI, Vilà M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol 22:151–163. https://doi.org/10.1111/gcb.1300

    Article  Google Scholar 

  • Gallien L, Carboni M (2017) The community ecology of invasive species: where are we and what’s next? Ecography 40:335–352

    Article  Google Scholar 

  • Gauff RPM, Lejeusne C, Arsenieff L et al (2022) Alien vs. predator: influence of environmental variability and predation on the survival of ascidian recruits of a native and alien species. Biol Invasions. https://doi.org/10.1007/s10530-021-02720-3

    Article  Google Scholar 

  • Giachetti CB, Battini N, Castro KL, Schwindt E (2020) Invasive ascidians: How predators reduce their dominance in artificial structures in cold temperate areas. J Exp Mar Biol Ecol 533:151459

    Article  Google Scholar 

  • Giachetti CB, Battini N, Castro KL, Schwindt E (2022) The smaller, the most delicious: differences on vulnerability to predation between juvenile and adult of invasive ascidians. Estuar Coast Shelf Sci 268:107810. https://doi.org/10.1016/j.ecss.2022.107810

    Article  Google Scholar 

  • Glasby TM, Connell SD (2007) Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions? Mar Biol 151:887–895

    Article  Google Scholar 

  • González A, Santelices B (2004) A dichotomous species of Codium (Bryopsidales, Chlorophyta) is colonizing northern Chile. Rev Chil Hist Nat 77:293–304

    Article  Google Scholar 

  • Hawkins SJ, Hartnoll RG (1985) Factors determining the upper limits of intertidal canopy-forming algae. Mar Ecol Prog Ser 20:265–272

    Article  Google Scholar 

  • Heger T, Jeschke JM (2014) The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123:741–750. https://doi.org/10.1111/j.1600-0706.2013.01263.x

    Article  Google Scholar 

  • Helmuth B, Broitman BR, Blanchette CA et al (2006) Mosaic patterns of thermal stress in the rocky intertidal zone: implications for climate change. Ecol Monogr 76:461–479

    Article  Google Scholar 

  • Hernández CE, Neill PE, Pulgar JM et al (2002) Water temperature fluctuations and territoriality in the intertidal zone: two possible explanations for the elevational distribution of body size in Graus nigra. J Fish Biol 61:472–488. https://doi.org/10.1111/j.1095-8649.2002.tb01578.x

    Article  Google Scholar 

  • Januario SM, Estay SA, Labra FA, Lima M (2015) Combining environmental suitability and population abundances to evaluate the invasive potential of the tunicate Ciona intestinalis along the temperate South American coast. PeerJ 3:e1357. https://doi.org/10.7717/peerj.1357

    Article  PubMed  PubMed Central  Google Scholar 

  • Jofré-Madariaga D, Rivadeneira MM, Tala F, Thiel M (2014) Environmental tolerance of the two invasive species Ciona intestinalis and Codium fragile: their invasion potential along a temperate coast. Biol Invasions 16:2507–2527. https://doi.org/10.1007/s10530-014-0680-7

    Article  Google Scholar 

  • Kim JK, Yarish C, Pereira R (2016) Tolerances to hypo-osmotic and temperature stresses in native and invasive species of Gracilaria (Rhodophyta). Phycologia 55:257–264. https://doi.org/10.2216/15-90.1

    Article  Google Scholar 

  • Kimbro DL, Cheng BS, Grosholz ED (2013) Biotic resistance in marine environments. Ecol Lett 16:821–833

    Article  PubMed  Google Scholar 

  • Kincaid ES, Rivera CE (2021) Predators associated with marinas consume indigenous over non-indigenous ascidians. Estuar Coasts 44:579–588. https://doi.org/10.1007/s12237-020-00793-2

    Article  Google Scholar 

  • Leclerc JC, Viard F, González Sepúlveda EG et al (2019) Habitat type drives the distribution of non-indigenous species in fouling communities regardless of associated maritime traffic. Divers Distrib 26:62–75

    Article  Google Scholar 

  • Leclerc JC, Viard F, Brante A (2020) Experimental and survey-based evidences for effective biotic resistance by predators in ports. Biol Invasions 22:339–352

    Article  Google Scholar 

  • Legrand E, Riera P, Pouliquen L et al (2018) Ecological characterization of intertidal rockpools: seasonal and diurnal monitoring of physico-chemical parameters. Reg Stud Mar Sci 17:1–10. https://doi.org/10.1016/j.rsma.2017.11.003

    Article  Google Scholar 

  • Lenz M, da Gama BAP, Gerner NV et al (2011) Non-native marine invertebrates are more tolerant towards environmental stress than taxonomically related native species: Results from a globally replicated study. Environ Res 111:943–952. https://doi.org/10.1016/j.envres.2011.05.001

    Article  CAS  PubMed  Google Scholar 

  • Lorenzen S (2007) The limpet Patella vulgata L. at night in air: effective feeding on Ascophyllum nodosum monocultures and stranded seaweeds. J Molluscan Stud 73:267–274

    Article  Google Scholar 

  • Lyons DA, Van Alstyne KL, Scheibling RE (2007) Anti-grazing activity and seasonal variation of dimethylsulfoniopropionate-associated compounds in the invasive alga Codium fragile ssp. tomentosoides. Mar Biol 153:179–188. https://doi.org/10.1007/s00227-007-0795-9

    Article  CAS  Google Scholar 

  • McKnight E, García-Berthou E, Srean P, Rius M (2017) Global meta-analysis of native and nonindigenous trophic traits in aquatic ecosystems. Glob Change Biol 23:1861–1870

    Article  Google Scholar 

  • Menge BA (1978) Predation intensity in a rocky intertidal community. Oecologia 3:17–35

    Article  Google Scholar 

  • Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757

    Article  Google Scholar 

  • Muñoz AA, Ojeda FP (1997) Feeding guild structure of a rocky intertidal fish assemblage in central Chile. Environ Biol Fishes 49:471–479. https://doi.org/10.1023/A:1007305426073

    Article  Google Scholar 

  • Musrri CA, Poore AGB, Hinojosa IA et al (2019) Variation in consumer pressure along 2500 km in a major upwelling system: crab predators are more important at higher latitudes. Mar Biol 166:142. https://doi.org/10.1007/s00227-019-3587-0

    Article  Google Scholar 

  • Navarrete SA, Castilla JC (2003) Experimental determination of predation intensity in an intertidal predator guild: dominant versus subordinate prey. Oikos 100:251–262. https://doi.org/10.1034/j.1600-0706.2003.11996.x

    Article  Google Scholar 

  • Neill PE, Alcalde O, Faugeron S et al (2006) Invasion of Codium fragile ssp. tomentosoides in northern Chile: a new threat for Gracilaria farming. Aquaculture 259:202–210. https://doi.org/10.1016/j.aquaculture.2006.05.009

    Article  Google Scholar 

  • Osman RW, Whitlatch RB (2004) The control of the development of a marine benthic community by predation on recruits. J Exp Mar Biol Ecol 311:117–145

    Article  Google Scholar 

  • Pack KE, Rius M, Mieszkowska N (2021) Long-term environmental tolerance of the non-indigenous Pacific oyster to expected contemporary climate change conditions. Mar Environ Res 164:105226. https://doi.org/10.1016/j.marenvres.2020.105226

    Article  CAS  PubMed  Google Scholar 

  • Papacostas K, Rielly-Carroll E, Georgian S et al (2017) Biological mechanisms of marine invasions. Mar Ecol Prog Ser 565:251–268. https://doi.org/10.3354/meps12001

    Article  Google Scholar 

  • Pincebourde S, Sanford E, Helmuth B (2008) Body temperature during low tide alters the feeding performance of a top intertidal predator. Limnol Oceanogr 53:1562–1573

    Article  Google Scholar 

  • Pintor LM, Byers JE (2015) Do native predators benefit from non-native prey? Ecol Lett 18:1174–1180

    Article  PubMed  Google Scholar 

  • Prince JS, LeBlanc WG (1992) Comparative feeding preference of Strongylocentrotus droebachiensis (Echinoidea) for the invasive seaweed Codium fragile ssp. tomentosoides (Chlorophyceae) and four other seaweeds. Mar Biol 113:159–163. https://doi.org/10.1007/BF00367649

    Article  Google Scholar 

  • Prior KM, Powell THQ, Joseph AL, Hellmann JJ (2015) Insights from community ecology into the role of enemy release in causing invasion success: the importance of native enemy effects. Biol Invasions 17:1283–1297. https://doi.org/10.1007/s10530-014-0800-4

    Article  Google Scholar 

  • Pulgar JM, Bozinovic F, Ojeda FP (2005) Local distribution and thermal ecology of two intertidal fishes. Oecologia 142:511–520. https://doi.org/10.1007/s00442-004-1755-4

    Article  PubMed  Google Scholar 

  • Rahn DA, Garreaud RD, Rutllant JA (2011) The low-level atmospheric circulation near Tongoy-Bay point Lengua de Vaca (Chilean Coast, 30 degrees S). MWR 139:3628–3647

    Article  Google Scholar 

  • Renault L, Dewitte B, Marchesiello P et al (2012) Upwelling response to atmospheric coastal jets off central Chile: a modeling study of the October 2000 event. J Geophys Res. https://doi.org/10.1029/2011JC007446

    Article  Google Scholar 

  • Ricciardi A, Hoopes MF, Marchetti MP, Lockwood JL (2013) Progress toward understanding the ecological impacts of nonnative species. Ecol Monogr 83:263–282

    Article  Google Scholar 

  • Riquelme-Pérez N, Musrri CA, Stotz WB et al (2019) Coastal fish assemblages and predation pressure in northern-central Chilean Lessonia trabeculata kelp forests and barren grounds. PeerJ 7:e6964

    Article  PubMed  PubMed Central  Google Scholar 

  • Rius M, Potter EE, Aguirre JD, Stachowicz JJ (2014) Mechanisms of biotic resistance across complex life cycles. J Anim Ecol 83:296–305

    Article  PubMed  Google Scholar 

  • Rivadeneira M, Fernández M, Navarrete S (2002) Latitudinal trends of species diversity in rocky intertidal herbivore assemblages: spatial scale and the relationship between local and regional species richness. Mar Ecol Prog Ser 245:123–131. https://doi.org/10.3354/meps245123

    Article  Google Scholar 

  • Robinson TB, Pope HR, Hawken L, Binneman C (2015) Predation-driven biotic resistance fails to restrict the spread of a sessile rocky shore invader. Mar Ecol Prog Ser 522:169–179

    Article  Google Scholar 

  • Rodríguez SR (2003) Consumption of drift kelp by intertidal populations of the sea urchin Tetrapygus niger on the central Chilean coast: possible consequences at different ecological levels. Mar Ecol Prog Ser 251:141–151

    Article  Google Scholar 

  • Rogers TL, Byrnes JE, Stachowicz JJ (2016) Native predators limit invasion of benthic invertebrate communities in Bodega Harbor, California, USA. Mar Ecol Prog Ser 545:161–173

    Article  Google Scholar 

  • Sareyka J, Kraufvelin P, Lenz M et al (2011) Differences in stress tolerance and brood size between a non-indigenous and an indigenous gammarid in the northern Baltic Sea. Mar Biol 158:2001–2008. https://doi.org/10.1007/s00227-011-1708-5

    Article  Google Scholar 

  • Scheibling R, Anthony S (2001) Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides. Mar Biol 139:139–146. https://doi.org/10.1007/s002270100567

    Article  Google Scholar 

  • Scheibling R, Gagnon P (2006) Competitive interactions between the invasive green alga Codium fragile ssp. tomentosoides and native canopy-forming seaweeds in Nova Scotia (Canada). Mar Ecol Prog Ser 325:1–14

    Article  Google Scholar 

  • Scheibling R, Lyons DA, Sumi CBT (2008) Grazing of the invasive alga Codium fragile ssp. tomentosoides by the common periwinkle Littorina littorea: Effects of thallus size, age and condition. J Exp Mar Biol Ecol 355:103–113. https://doi.org/10.1016/j.jembe.2007.12.002

    Article  Google Scholar 

  • Schmidt AL, Scheibling RE (2005) Population dynamics of an invasive green alga, Codium fragile subsp. tomentosoides, in tidepools on a rocky shore in Nova Scotia, Canada. Écoscience 12:403–411. https://doi.org/10.2980/i1195-6860-12-3-403.1

    Article  Google Scholar 

  • Schultheis EH, Berardi AE, Lau JA (2015) No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology 96:2446–2457. https://doi.org/10.1890/14-2158.1

    Article  PubMed  Google Scholar 

  • Selwood KE, Zimmer HC (2020) Refuges for biodiversity conservation: a review of the evidence. Biol Conserv 245:108502

    Article  Google Scholar 

  • Shenkar N, Shmuel Y, Huchon D (2018) The invasive ascidian Ciona robusta recorded from a Red Sea marina. Mar Biodivers 48:2211–2214

    Article  Google Scholar 

  • Simkanin C, Dower JF, Filip N et al (2013) Biotic resistance to the infiltration of natural benthic habitats: Examining the role of predation in the distribution of the invasive ascidian Botrylloides violaceus. J Exp Mar Biol Ecol 439:76–83

    Article  Google Scholar 

  • Simoncini M, Miller RJ (2007) Feeding preference of Strongylocentrotus droebachiensis (Echinoidea) for a dominant native ascidian, Aplidium glabrum, relative to the invasive ascidian Botrylloides violaceus. J Exp Mar Biol Ecol 342:93–98. https://doi.org/10.1016/j.jembe.2006.10.019

    Article  Google Scholar 

  • Sumi C, Scheibling R (2005) Role of grazing by sea urchins Strongylocentrotus droebachiensis in regulating the invasive alga Codium fragile ssp. tomentosoides in Nova Scotia. Mar Ecol Prog Ser 292:203–212. https://doi.org/10.3354/meps292203

    Article  Google Scholar 

  • Thompson RC, Norton TA, Hawkins SJ (2004) Physical stress and biological control regulate the producer–consumer balance in intertidal biofilms. Ecology 85:1372–1382

    Article  Google Scholar 

  • Trowbridge CD (1995) Establishment of the green alga Codium fragile ssp. tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. J Ecol 83:949. https://doi.org/10.2307/2261177

    Article  Google Scholar 

  • Trowbridge CD (2002) Local elimination of Codium fragile ssp. tomentosoides: indirect evidence of sacoglossan herbivory? JMBA 82:1029–1030

    Google Scholar 

  • Underwood AJ, Jernakoff P (1984) The effects of tidal height, wave-exposure, seasonality and rock-pools on grazing and the distribution of intertidal macroalgae in New South Wales. J Exp Mar Biol Ecol 75:71–96

    Article  Google Scholar 

  • Uribe E, Etchepare I (2002) Effects of biofouling by Ciona intestinalis on suspended culture of Argopecten purpuratus in Bahía Inglesa, Chile. Bull Aquac Assoc Can 102:93–95

    Google Scholar 

  • Valdivia N, González AE, Manzur T, Broitman BR (2013) Mesoscale variation of mechanisms contributing to stability in rocky shore communities. PLoS One 8:e54159. https://doi.org/10.1371/journal.pone.0054159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Véliz K, Chandía N, Bischof K, Thiel M (2020) Geographic variation of UV stress tolerance in red seaweeds does not scale with latitude along the SE Pacific coast. J Phycol 56:1090–1102

    Article  PubMed  Google Scholar 

  • Vermeij MJA, Smith TB, Dailer ML, Smith CM (2009) Release from native herbivores facilitates the persistence of invasive marine algae: a biogeographical comparison of the relative contribution of nutrients and herbivory to invasion success. Biol Invasions 11:1463–1474. https://doi.org/10.1007/s10530-008-9354-7

    Article  Google Scholar 

  • Wallenstein FM, Peres SD, Xavier ED, Neto AI (2010) Phytobenthic communities of intertidal rock pools in the eastern islands of Azores and their relation to position on shore and pool morphology. Arquipel Life Mar Sci 27:9–20

    Google Scholar 

  • Whalen MA, Whippo RDB, Stachowicz JJ et al (2020) Climate drives the geography of marine consumption by changing predator communities. Proc Natl Acad Sci USA 117:28160–28166. https://doi.org/10.1073/pnas.2005255117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilcove DS, Rothstein D, Dubow J et al (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615. https://doi.org/10.2307/1313420

    Article  Google Scholar 

  • Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666. https://doi.org/10.2307/2265769

    Article  Google Scholar 

  • Wing SR, Leichter JJ (2011) Variation in environmental conditions in a subtidal prey refuge: effects of salinity stress, food availability and predation on mussels in a fjord system. Mar Ecol Prog Ser 422:201–210

    Article  Google Scholar 

  • Zerebecki RA, Sorte CJB (2011) Temperature tolerance and stress proteins as mechanisms of invasive species success. PLoS One 6:e14806. https://doi.org/10.1371/journal.pone.0014806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all members of the BEDIM laboratory at UCN for their support during this study. The constructive comments from three anonymous reviewers helped substantially to improve the original version of this manuscript, for which we are grateful.

Funding

Financial support was provided by the ANID-FONDECYT 1190954 to MT and MA, and by the Anid-Fondecyt Postdoctorado 3201074 to SR.

Author information

Authors and Affiliations

Authors

Contributions

MT conceived the idea; MT designed the experiment; MT, RMA, DJM, OP and SR performed the experiment; MAA analyzed the data; ER and MT led the writing of the manuscript. MAA contributed critically to the drafts and all authors gave final approval for publication.

Corresponding author

Correspondence to Martin Thiel.

Ethics declarations

Conflict of interest

The authors declare to have no conflict of interest.

Ethical approval

The algae and tunicates were collected under the permit CEC UCN 10–2019 by the Scientific Ethics Committee of Universidad Católica del Norte.

Additional information

Responsible Editor: R.N. Cuthbert.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 298 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rothäusler, E., Aguilera, M.A., Arias, R.M. et al. Herbivore and predator pressure in tidepools along an intertidal gradient: no consumption refuge for invasive species!. Mar Biol 169, 134 (2022). https://doi.org/10.1007/s00227-022-04114-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-022-04114-y

Keywords

Navigation