Skip to main content

Advertisement

Log in

Utilization of invasive tamarisk by salt marsh consumers

  • Plant-Animal Interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Plant invasions of coastal wetlands are rapidly changing the structure and function of these systems globally. Alteration of litter dynamics represents one of the fundamental impacts of an invasive plant on salt marsh ecosystems. Tamarisk species (Tamarix spp.), which extensively invade terrestrial and riparian habitats, have been demonstrated to enter food webs in these ecosystems. However, the trophic impacts of the relatively new invasion of tamarisk into marine ecosystem have not been assessed. We evaluated the trophic consequences of invasion by tamarisk for detrital food chains in the Tijuana River National Estuarine Research Reserve salt marsh using litter dynamics techniques and stable isotope enrichment experiments. The observations of a short residence time for tamarisk combined with relatively low C:N values indicate that tamarisk is a relatively available and labile food source. With an isotopic (15N) enrichment of tamarisk, we demonstrated that numerous macroinvertebrate taxonomic and trophic groups, both within and on the sediment, utilized 15N derived from labeled tamarisk detritus. Infaunal invertebrate species that took up no or limited 15N from labeled tamarisk (A. californica, enchytraeid oligochaetes, coleoptera larvae) occurred in lower abundance in the tamarisk-invaded environment. In contrast, species that utilized significant 15N from the labeled tamarisk, such as psychodid insects, an exotic amphipod, and an oniscid isopod, either did not change or occurred in higher abundance. Our research supports the hypothesis that invasive species can alter the trophic structure of an environment through addition of detritus and can also potentially impact higher trophic levels by shifting dominance within the invertebrate community to species not widely consumed.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Able KW, Hagan SM, Brown SA (2003) Mechanisms of marsh habitat alteration due to Phragmites: response of young-of-the-year mummichog (Fundulus heteroclitus) to treatment for Phragmites removal. Estuaries 26:484–494

    Article  Google Scholar 

  • Ashton IW, Hyatt LA, Howe KM, Gurevitch J, Lerdau MT (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272

    Article  Google Scholar 

  • Ayres DR, Smith DL, Zaremba K, Klohr S, Strong DR (2003) Spread of exotic cordgrasses and hybrids (Spartina sp.) in the tidal marshes of San Francisco Bay, CA, USA. Biol Invasions 6:221–231

    Article  Google Scholar 

  • Bailey JK, Schweitzer JA, Whitham TG (2001) Salt cedar negatively affects biodiversity of aquatic macroinvertebrates. Wetlands 21:442–447

    Article  Google Scholar 

  • Baum BR (1978) The Genus Tamarix. Israel Academy of Sciences and Humanities, Jerusalem

    Google Scholar 

  • Bickel DJ, Dyte CE (1989) Family Dolichopodidae. In: Evenhuis NL (ed) A catalog of Australasian and Oceanian Diptera. Brill, Leiden, pp 398–418

  • Blanchard G, Ghretiennot-Dinet MJ, Dinet A, Robert JM (1988) A simplified method for sorting microphytobenthos from sediments using Ludox Silica-sol. C R Acad Sci Biol Mar 307:569–576

    Google Scholar 

  • Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 201–221

    Google Scholar 

  • Carefoot TH (1973) Feeding, food preference, and the uptake of food energy by the supralittoral isopod Ligia pallasii. Mar Biol 18:228–236

    Article  Google Scholar 

  • Carman KR, Fry B (2002) Small-sample methods for delta C-13 and delta N-15 analysis of the diets of marsh meiofaunal species using natural-abundance and tracer-addition isotope techniques. Mar Ecol Prog Ser 121:99–116

    Google Scholar 

  • Chambers RM, Osgood DT, Bart DJ, Montalto F (2003) Phragmites australis invasion and expansion in tidal wetlands: interactions among salinity, sulfide, and hydrology. Estuaries 26:396–406

    Article  Google Scholar 

  • Chapin FS, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277:500–504

    Article  CAS  Google Scholar 

  • Chapman JW, Dorman JA (1975) Diagnosis, systematics, and notes on Grandidierella japonica (Amphipoda: Gammaridea) and its introduction to the Pacific Coast of the United States. Bull South Calif Acad Sci 74:104–108

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation. Natural Environment Research Council, Plymouth Marine Laboratory, Plymouth

    Google Scholar 

  • Crooks JA (2002) Characterizing the consequences of invasions: the role of introduced ecosystem engineers. Oikos 97:153–166

    Article  Google Scholar 

  • Currin CA, Newell SY, Pearl HW (1995) The role of standing dead Spartina alterniflora and benthic microalgae in salt marsh food webs: considerations based on multiple stable isotope analysis. Mar Ecol Prog Ser 121:99–116

    Article  Google Scholar 

  • Dash MC, Cragg JB (1972) Selection of microfungi by Enchytraidae (Oilgochaeta) and other members of the soil fauna. Pedobiology 12:282–286

    Google Scholar 

  • Di Sabatino A, Gerecke R, Martin P (2000) The biology and ecology of lotic water mites (Hydrachnidia). Freshw Biol 44:47–62

    Article  Google Scholar 

  • Di Tomaso JM (1998) Impact, biology, and ecology of saltcedar (Tamarix spp.) in the southwestern United States. Weed Technol 12:326–336

    Google Scholar 

  • Ellis LM, Crawford CS, Molles MC (1998) Comparison of litter dynamics in native and exotic riparian vegetation along the Middle Rio Grande of central New Mexico, U.S.A. J Arid Environ 38:283–296

    Article  Google Scholar 

  • Friedman JM, Auble GT, Shafroth PB, Scott ML, Merigliano MF, Freehling MD, Griffen ER (2005) Dominance of non-native riparian trees in western US. Biol Invasions 7:747–751

    Article  Google Scholar 

  • Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Continental Mar Sci 27:13–47

    CAS  Google Scholar 

  • Fry B, Wainwright SC (1991) Diatom sources of 13C-rich carbon in marine food webs. Mar Ecol Prog Ser 76:149–157

    Article  Google Scholar 

  • Greenstein DJ, Tiefenthaler LL (1997) Reproduction and population dynamics of a population of Grandidierella japonica (Stephensen) (Crustacea: Amphipoda) in Upper Newport Bay, California. Bull South Calif Acad Sci 96:34–42

    Google Scholar 

  • Grosholz ED (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27

    Article  Google Scholar 

  • Herman PMJ, Middelburg JJ, Widdows J, Lucas CH, Heip CHR (2000) Stable isotopes as trophic tracers: combining field sampling and manipulative labeling of food resources for macrobenthos. Mar Ecol Prog Ser 204:79–92

    Article  CAS  Google Scholar 

  • Herrera AM, Dudley TL (2003) Reduction of riparian arthropod abundance and diversity as a consequence of giant reed (Arundo donax) invasion. Biol Invasions 5:167–177

    Article  Google Scholar 

  • Kennedy TA, Finlay JC, Hobbie SE (2005) Eradication of invasive Tamarix ramosissima along a desert stream increases native fish density. Ecol Appl 15:2072–2083

    Article  Google Scholar 

  • Kennedy TA, Hobbie SE (2004) Saltcedar (Tamarix ramosissima) invasion alters organic matter dynamics in a desert stream. Freshw Biol 49:65–76

    Article  Google Scholar 

  • Kwak TJ, Zedler JB (1997) Food web analysis of southern California coastal wetlands using multiple stable isotopes. Oecologia 110:262–277

    Article  Google Scholar 

  • Levin LA, Talley TS, Hewitt J (1998) Macrobenthos of Spartina foliosa (Pacific cordgrass) salt marshes in Southern California: community structure and comparison to a Pacific mudflat and a Spartina alterniflora (Atlantic smooth cordgrass) marsh. Estuaries 21:129–144

    Article  Google Scholar 

  • Levin LA, Talley TS (2000) Influences of vegetation and abiotic environmental factors on salt marsh benthos. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Kluwer, Amsterdam, pp 661–708

    Google Scholar 

  • Levin LA, Currin CA (2005) Recovery of trophic function in restored Pacific wetlands. CA Sea Grant College program. Research completion report (UCSD). Paper Coastal 04–04

  • Levin LA, Neira C, Grosholz ED (2006) Invasive cordgrass modifies wetland trophic function. Ecology 87:419–432

    Article  PubMed  Google Scholar 

  • McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • Moore JC, Berlow E, Coleman D, de Ruiter C, Dong Q, Hastings A, Collins Johnson N, McCann K, Melville K, Morin P, Nadelhoffer K, Rosemond A, Post D, Sabo J, Scow K, Vanni M, Wall D (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600

    Article  Google Scholar 

  • Morisette JT, Jarnevich CS, Ullah A, Cai W, Pedelty JA, Gentle JE, Stohlgren TJ, Schnase JL (2006) A tamarisk habitat suitability map for the continental US. Front Ecol Envi 4:11–17

    Article  Google Scholar 

  • Moseman S, Levin LA, Currin C, Forder C (2004) Infaunal colonization, succession, & nutrition in a newly restored wetland at Tijuana Estuary, CA. Est Coast Shelf Sci 60:755–770

    Article  Google Scholar 

  • Neira C, Levin LA, Grosholz ED (2005) Benthic macrofaunal communities of three sites in San Francisco Bay invaded by hybrid Spartina, with comparison to uninvaded habitats. Mar Ecol Prog Ser 292:111–126

    Article  CAS  Google Scholar 

  • Neira C, Grosholz ED, Levin LA, Blake R (2006) Mechanisms generating modification of benthos following tidal flat invasion by a Spartina hybrid. Ecol Appl 16:1391–1404

    Article  PubMed  Google Scholar 

  • Neira C, Levin LA, Grosholz ED, Mendoza G (2007) Influence of invasive Spartina growth stages on associated macrofaunal communities. Biol Invasions 9:975–993

    Article  Google Scholar 

  • Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44:322–331

    Article  Google Scholar 

  • Osgood DT, Yozzo DJ, Chambers RM, Jacabson D, Hoffman T, Wnek J (2003) Tidal hydrology and habitat utilization by resident nekton in Phragmites and non-Phragmites marshes. Estuaries 26:522–533

    Article  Google Scholar 

  • Pennings SC, Carefoot TH, Siska EL, Chase ME, Page TA (1998) Feeding preferences of a generalist salt marsh crab: relative importance of multiple plant traits. Ecology 79:1968–1979

    Article  Google Scholar 

  • Petersen BJ, Howarth RW, Garritt RH (1985) Multiple stable isotopes used to trace the flow of organic matter in estuarine food webs. Science 227:1361–1363

    Article  Google Scholar 

  • Posey MH (1988) Community changes associated with the spread of an introduced seagrass, Zostera japonica. Ecology 69:974–983

    Article  Google Scholar 

  • Rooth JE, Stevenson JC, Cornwell JC (2003) Increased sediment accretion following invasion by Phragmites australis: the role of litter. Estuaries 26:476–483

    Article  Google Scholar 

  • Schlein Y, Muller G (1995) Assessment of plant tissue feeding by sand flies (Diptera: Psychodidae) and mosquitoes (Diptera: Culicidae). J Med Entomol 32:882–887

    PubMed  CAS  Google Scholar 

  • Stein BA, Flack SR (eds) (1996) America’s least wanted: alien species invasions of U.S. ecosystems. The Nature Conservancy, Arlington, Virginia

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Stevens LE (2000) A synthesis on the ecology and management of saltcedar (Tamaricaceae: Tamarix ramosissima), with emphasis on the Grand Canyon region: final progress report. Grand Canyon Wildlands Council, Flagstaff

  • Talley TS, Levin LA (1999) Macrofaunal succession and community structure in Salicornia marshes of southern California. Est Coast Shelf Sci 49:713–731

    Article  Google Scholar 

  • Talley TS, Levin LA (2001) Modification of sediments and macrofauna by an invasive marsh plant. Biol Invasions 3:51–68

    Article  Google Scholar 

  • Twilley RR, Pozo M, Garcia VH, Rivera-Monroy VH, Zambrano R, Bodero A (1997) Litter dynamics in riverine mangrove forests in the Guayas River estuary, Ecuador. Oecologia 111:109–122

    Article  Google Scholar 

  • van Oevelen D, Moodley L, Soetaert K, Middelburg JJ (2006) The trophic significance of bacterial carbon in a marine intertidal sediment: results of an in situ stable isotope labeling study. Limnol Oceanog 51:2349–2359

    Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:629–663

    Article  CAS  Google Scholar 

  • Wavre M, Brinkhurst BO (1971) Interactions between some tubificid oligochaetes and bacteria found in the sediments of Toronto Harbor. J Fish Res Board Can 28:335–341

    Google Scholar 

  • Webster JR, Benfield EF (1986) Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst 17:567–594

    Article  Google Scholar 

  • West JM, Williams GD, Madon SP, Zedler JB (2003) Integrating spatial and temporal variability into analysis of fish food web linkages in Tijuana Estuary. Environ Biol Fish 67:297–309

    Article  Google Scholar 

  • Whitcraft CR (2007) Wetland plant influence on sediment ecosystem structure and trophic function. Diss. Scripps Institution of Oceanography, UCSD, 2007

  • Whitcraft CR, Levin LA (2007) Regulation of benthic algal and animal communities by salt marsh plants: impact of shading. Ecology 88:904–917

    Article  PubMed  Google Scholar 

  • Whitcraft CR, Talley DM, Crooks JA, Boland J, Gaskin J (2007) Invasion of tamarisk (Tamarix spp.) in a southern California salt marsh. Biol Invasions 9:875–879

    Article  Google Scholar 

  • White DS, Howes BL (1994) Nitrogen incorporation into decomposing tissue litter of Spartina alterniflora. Limnol Oceanogr 39:629–633

    Google Scholar 

  • Williams GD, West JM, Zedler JB (2001) Shifts in fish and invertebrate assemblages of two southern California estuaries during the 1997–98 El Nino. Bull South Calif Acad Sci 100:212–226

    Google Scholar 

  • Zajac RN, Whitlatch RB (1982) Response of estuarine infauna to disturbance II. Spatial and temporal variation of succession. Mar Ecol Prog Ser 10:15–27

    Article  Google Scholar 

  • Zavaleta E (2000) Valuing ecosystem services lost to Tamarix invasion. In: Mooney HA, Hobbs RJ (eds) Invasive species in a changing world. Island Press, Washington, D.C, pp 261–299

    Google Scholar 

  • Zedler JB, Nordby CS, Kus BE (1992) The ecology of Tijuana Estuary. NOAA Office of Coastal Resource Management, Washington D.C

    Google Scholar 

Download references

Acknowledgments

We thank the staff of Tijuana River National Estuarine Research Reserve (NERR), field assistants and laboratory helpers, especially P. McMillan, G. Mendoza, J. Gonzalez, J. Fodrie, J. Leddick, L. Pierotti, J. Hart, L. Warner-Lara, E. Kim, K. McFarland, M. Cordrey, M. Kiener, and C. Cody. D. Harris and the UC Davis Stable Isotope Facility provided prompt and accurate isotope analyses. Thanks also to C. Neira, T. Talley, and anonymous reviewers for helpful comments on the manuscript. This research was supported by the National Sea Grant College Program of the U.S. Department of Commerce’s NOAA Grants R/CZ 173 and R/CZ 190C through the CA Sea Grant and by the CA State Resources Agency, by the Edna Bailey Sussman fund, by CEQI Grant to LAL 06-000531-02, by the National Science Foundation under Grant OCE 0333444, by 2006 Space Grant (CalSpace), by a San Diego Foundation Blasker Grant, and by the Western Regional Panel of the Aquatic Nuisance Species Task Force. The views expressed herein do not necessarily reflect the views of those organizations. Access to the study site was granted by the NOAA NERR and US Fish and Wildlife Service.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christine R. Whitcraft.

Additional information

Communicated by Barbara Downes.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Whitcraft, C.R., Levin, L.A., Talley, D. et al. Utilization of invasive tamarisk by salt marsh consumers. Oecologia 158, 259–272 (2008). https://doi.org/10.1007/s00442-008-1144-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-1144-5

Keywords

Navigation