Skip to main content
SpringerLink
Log in

Similar dietary but different numerical responses to nonnative tamarisk (Tamarix spp.) by two native warblers

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Native species can have a range of responses to nonnative introductions, from negative to positive, and understanding how and why native species respond differently to nonnatives remains an important management challenge. Based on differences and similarities in ecology and behavior, we predicted how abundance and diet of two native warblers, Lucy’s warbler (Oreothlypis luciae) and yellow warbler (Setophaga petechia), would differ in habitats with different amounts of nonnative tamarisk trees and the three nonnative insects obligately dependent on tamarisk (Tamarix spp.). Specifically, we predicted that Lucy’s warblers would have similar densities across sites, yellow warbler densities would be inversely related to tamarisk cover, and both warblers, being generalist insectivores, would incorporate tamarisk biocontrol insects in their diet. Based on point counts and fecal samples at six sites along the Virgin River in the southwestern United States, we found that yellow warblers decreased in abundance with increasing tamarisk cover, while Lucy’s warbler abundance did not and that diet of the two warblers did not differ, with both species exhibiting strong selection for the nonnative tamarisk weevil (Coniatus splendidulus) and weak to no selection for the nonnative tamarisk leafhopper (Opsius stactogalus). Both warblers showed negative selection for the tamarisk beetle (Diorhabda carinulata) and its larvae, even when those insects were 10–100 times more abundant during outbreaks. Although both warblers exploited the novel food resources offered by tamarisk, with those insects contributing half or more of total prey biomass, Lucy’s warblers were better able to maintain densities in tamarisk habitats. We hypothesize this was due to the Lucy’s warbler’s ability to exploit a broader array of habitats surrounding tamarisk sites and its cavity nesting habit that buffers its nests from the higher temperatures and lower humidity of tamarisk-dominated habitat. Our results suggest that predictions based on detailed knowledge of the form and function of native and nonnative species can be used to predict native bird response to nonnatives.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson BW, Ohmart RD (1977) Vegetation structure and bird use in the lower Colorado River Valley. In: Johnson RR, Jones DA (ed) Importance, preservation and management of riparian habitat: A symposium. General Technical Report RM-166. US Forest Service, Colorado, pp 23–34

  • Barber NA, Marquis RJ, Tori WP (2008) Invasive prey impacts the abundance and distribution of native predators. Ecology 89:2678–2683

    Article  PubMed  Google Scholar 

  • Bateman HL, Johnson MJ (2015) Effects of biocontrol and restoration on wildlife in Southwestern riparian habitats. Report submitted to Southern Rockies and Desert Landscape Conservation Cooperative

  • Bateman HL and Paxton EH (2010) Saltcedar and Russian olive interactions with wildlife. In: Shafroth PB, Brown CS, Merritt DM (eds) Saltcedar and Russian olive control and demonstration act science assessment, US Geological Survey Scientific Investigations Report 2009–5247, pp 51–59

  • Bateman HL, Paxton EH, Longland WS (2013) Tamarix as wildlife habitat. In: Sher A, Quigley MF (eds) Tamarix: a case study of ecological change in the American west. Oxford University Press, Oxford, pp 168–188

    Chapter  Google Scholar 

  • Bean DW, Dudley T, Hultine K (2013) Bring on the beetles! The history and impact of tamarisk biological control. In: Sher A, Quigley MF (eds) Tamarix: a case study of ecological change in the American west. Oxford University Press, Oxford, pp 377–403

    Chapter  Google Scholar 

  • Biermann GC, Sealy SG (1982) Parental feeding of nestling yellow warblers in relation to brood size and prey availability. Auk 99:332–341

    Google Scholar 

  • Bloodworth BR, Shafroth PB, Sher AA, Manners RB, Bean DW, Johnson MJ, Hinojosa-Heurta O (2016) Tamarisk beetle (Diorhabda spp.) in the Colorado River basin: Synthesis of an expert panel forum. Scientific and Technical Report No. 1, Colorado, USA

  • Borror DJ, DeLong DM, Triplehorn CA, Johnson NF (2005) Borror and DeLong’s introduction to the study of insects. Thomson Brooks/Cole, California

    Google Scholar 

  • Bright DE, Kondratieff BC, Norton AP (2013) First record of the splendid tamarisk weevil, Coniatus splendidulus (F.) (Coleoptera: curculionidae: Hyperinae), in Colorado, USA. Coleopts Bull 67:302–303

    Article  Google Scholar 

  • Brush T, Anderson BW, Ohmart RD (1983) Habitat selection related to resource availability among cavity-nesting birds. In: Davis JW, Goodwin GA, Ockenfeis RA (eds) Snag habitat management: Proceedings of the symposium. General Technical Report RM-99, US Forest Service, Colorado, USA 88–98

  • Buckland ST, Anderson DR, Burnham KP, Laake JL, Borchers DL, Thomas L (2001) Introduction to distance sampling. Oxford University Press, Oxford

    Google Scholar 

  • Burger JC, Patten MA, Rotenberry JT, Redak RA (1999) Foraging ecology of the California gnatcatcher deduced from fecal samples. Oecologia 120:304–310

    Article  PubMed  Google Scholar 

  • Busby DG, Sealy SG (1979) Feeding ecology of a population of nesting Yellow warblers. Can J Zool 57:1670–1681

    Article  Google Scholar 

  • Carlisle JD, Holberton RL (2006) Relative efficiency of fecal versus regurgitated samples for assessing diet and the deleterious effects of tartar emetic on migratory birds. J Field Ornithol 77:126–135

    Article  Google Scholar 

  • Chew MK (2009) The monstering of tamarisk: how scientists made a plant into a problem. J Hist Biol 42:231–266

    Article  PubMed  Google Scholar 

  • Cody ML (1974) Competition and the structure of bird communities. Princeton University Press, New Jersey

    Google Scholar 

  • De Graaf RM, Tilghman NG, Anderson SH (1985) Foraging guilds of North American birds. Environ Manag 9:493–536

    Article  Google Scholar 

  • Dennison PE, Nagler PL, Hultine KR, Glenn EP, Ehleringer JR (2009) Remote monitoring of tamarisk defoliation and evapotranspiration following saltcedar leaf beetle attack. Remote Sens Environ 113:1462–1472

    Article  Google Scholar 

  • Drabu S, Chaturvedi S, Sharma A (2012) Tamarix gallica-An overview. Asian J Pharm Clin Res 5:17–19

    Google Scholar 

  • Dudley TL, DeLoach CJ (2004) Saltcedar (Tamarix spp.), endangered species, and biological weed control—can they mix? Weed Technol 18:1542–1551

    Article  Google Scholar 

  • Durst SL, Theimer TC, Paxton EH, Sogge MK (2008) Age, habitat, and yearly variation in the diet of a generalist insectivore, the southwestern willow flycatcher. Condor 110:514–525

    Article  Google Scholar 

  • Eckberg JR, Foster ME (2011) First account of the splendid tamarisk weevil, Coniatus splendidulus Fabricius, 1781 (Coleoptera: curculionidae) in Nevada. Pan-Pac Entomol 87:51–53

    Article  Google Scholar 

  • Ellis LM (1995) Bird use of saltcedar and cottonwood vegetation in the Middle Rio Grande Valley of New Mexico, USA. J Arid Environ 30:339–349

    Article  Google Scholar 

  • Fornasari L (1998) Biology, ethology, and the impact on the host by Coniatus tamarisci (F.) (Coleoptera: curculionidae), a natural enemy of Tamarix spp. (Tamariacaceae, salcedar) in France. Biol Control 13:25–40

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Frydenhall MJ (1967) Feeding ecology and territorial behavior of the Yellow warbler. Dissertation, Utah State University

  • Gavin TA, Sowls LK (1975) Avian fauna of a San Pedro Valley mesquite forest. J Ariz Acad Sci 10:33–41

    Article  Google Scholar 

  • Harding L (1930) The biology of Opsius stactogalus Fieber (Homoptera, Cicadellidae). J Kans Entomol Soc 3:7–22

    Google Scholar 

  • Hunter WC, Ohmart RD, Anderson BW (1988) Use of exotic saltcedar (Tamarix chinensis) by birds in arid riparian systems. Condor 90:113–123

    Article  Google Scholar 

  • Jenni L, Retimann P, Jenni-Eiermann S (1990) Recognizability of different food types in faeces and in alimentary flushes of Sylvia warblers. Ibis 132:445–453

    Article  Google Scholar 

  • Kendeigh SM (1947) Bird population studies in the coniferous forest biome during a spruce budworm outbreak. Bull Dep Lands For Ontario, Canada. Div Res Biol 1:1–100

    Google Scholar 

  • Kleintjes PK, Dahlsten DL (1992) A comparison of three techniques for analyzing diet of plain titmouse and chestnut-backed nestling (Camparacion de tres tecnicas para analizar la utilizacion de arthropods en la dieta de pichones de Parus inomatus y P. rufescens). J Field Ornithol 63:276–285

    Google Scholar 

  • Knopf FL (1988) Conservation of steppe birds in North America. Ecol Conserv Grassl Birds 7:27–41 (ICBP technical publication)

    Google Scholar 

  • Landres PB, MacMahon JA (1980) Guilds and community organization: analysis of an oak woodland avifauna in Sonora, Mexico. Auk 97:351–365

    Google Scholar 

  • Lewis PA, deLoach CJ, Knutson AE, Tracy JL, To Robbin (2003) Biology of Diorhabda elongata deserticola (Coleoptera: Chrysomelidae), an Asian leaf beetle for biological control of saltcedars (Tamarix spp.) in the United States. Biol Control 27:101–116

    Article  Google Scholar 

  • Longland W, Dudley T (2008) Effects of a biological control agent on the use of saltcedar habitat by passerine birds. Great Basin Birds 10:21–26

    Google Scholar 

  • Lowther PE, Celada C, Klein NK, Rimmer CC, Spector DA (1999) Yellow warbler (Setophaga petechia). In: Poole A, Gill F (eds) Birds of North America. The Birds of North America, Inc., Philadelphia, 454:1–32

  • Manly BFJ, McDonal LL, Thomas DL (1993) Resources selection by animals. Chapman and Hall, London

    Book  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • Meents JK, Rice J, Anderson BW, Ohmart RD (1983) Nonlinear relationships between birds and vegetation. Ecology 64:1022–1027

    Article  Google Scholar 

  • Michalski M, Nadolski J, Marciniak B, Loga B, Banbura J (2011) Faecal analysis as a method of nestling diet determination in insectivorous birds: a case study in blue tits Cyanistes caeruleus and great tits Parus major. ACTA Ornithol 46:164–172

    Article  Google Scholar 

  • Moran PJ, DeLoach CJ, Dudley TL, Sanabria J (2009) Open field host selection and behavior by tamarisk beetles (Diorhabda spp.) (Coleoptera: Chrysomelidae) in biological control of exotic saltcedars (Tamarix spp.) and risks to non-target athel (T. aphylla) and native Frankenia spp. Biol Control 50:243–261

    Article  Google Scholar 

  • Nagler PL, Glenn EP, Thompson TL, Huete A (2004) Leaf area index and normalized difference vegetation index as predictors of canopy characteristics and light interception by riparian species on the Lower Colorado River. Agric For Meteorol 125:1–17

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Package ‘vegan’. Community ecology package, version 2

  • Ortega YK, Greenwood LF, Callaway RM, Pearson DE (2014) Different responses of congeneric consumers to an exotic food resource: who gets the novel resource prize? Biol Invasions 16:1757–1767

    Article  Google Scholar 

  • Parrish J, Whitman M, Comings S (1994) A facilitated method for collection of fecal samples from mist–netted birds. N Am Bird Bander 19:49–51

    Google Scholar 

  • Pasteels JM (1993) The value of defensive compounds as taxonomic characters in the classification of leaf beetles. Biochem Syst Ecol 21:135–142

    Article  CAS  Google Scholar 

  • Paxton EH, Theimer TC, Sogge MK (2011) Tamarisk biocontrol using tamarisk beetles: potential consequences for riparian birds in the southwestern United States. Condor 113:255–265

    Article  Google Scholar 

  • Pearson DE (2009) Invasive plant architecture alters trophic interactions by changing predator abundance and behavior. Oecologia 159:549–558

    Article  PubMed  Google Scholar 

  • Pearson DE (2010) Trait and density mediated indirect interactions initiated by an exotic invasive plant autogenic ecosystem engineer. Am Nat 176:394–403

    Article  PubMed  Google Scholar 

  • Pearson DE, Callaway RM (2003) Indirect effects of host-specific biological control agents. Trends Ecol Evol 18:456–461

    Article  Google Scholar 

  • Pearson DE, Callaway RM (2005) Indirect nontarget effects of host-specific biological control agents: implications for biological control. Biol Control 35:288–298

    Article  Google Scholar 

  • Pearson DE, Callaway RM (2006) Biological control agents elevate hantavirus by subsidizing mice. Ecol Lett 9:442–449

    Article  Google Scholar 

  • Pearson DE, Callaway RM (2008) Weed biocontrol insects reduce native plant recruitment through second-order apparent competition. Ecol Appl 18:1489–1500

    Article  PubMed  Google Scholar 

  • Poulsen JG, Aebischer NJ (1995) Quantitative comparison of two methods assessing diet of nestling skylarks (Alauda arvensis). Auk 112:1070–1073

    Article  Google Scholar 

  • Puckett SL, van Riper C III (2014) Influences on the tamarisk leaf beetle (Diorhabda carinulata) on the diet of insectivorous birds along the Dolores River in southwestern Colorado. US Geological Survey Open-File Report 2014-1100 51 p

  • Pysek P, Jarosik V, Hulme PE, Pergl J, Hejda M, Schaffner U, Villa M (2012) A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Glob Change Biol 18:1725–1737

    Article  Google Scholar 

  • Ralph CP, Nagat SE, Ralph JC (1985) Analysis of droppings to describe diets of small birds. J Field Ornithol 2:165–175

    Google Scholar 

  • Reynolds RT, Scott JM, Nussbaum RA (1980) A variable circular-plot method for estimating bird numbers. Condor 82:309–313

    Article  Google Scholar 

  • Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939

    Article  Google Scholar 

  • Roemer GW, Donlan CJ, Courchamp F (2002) Golden eagles, feral pigs, and insular carnivores: how exotic species turn native predators into prey. PNAS 99:791–796

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg K, Cooper R (1990) Approaches to avian diet analysis. Stud Avian Biol 13:80–90

    Google Scholar 

  • Rosenberg KV, Ohmart RD, Hunter WC, Anderson BW (1991) Birds of the lower Colorado River valley. University of Arizona Press, Arizona

    Google Scholar 

  • Sih A, Stamps J, Yang LH, McElreath R, Ramenofsky M (2010) Behavior as a key component of integrative biology in a human-altered world. Integr Comp Biol 50:934–944

    Article  PubMed  Google Scholar 

  • Smith JN, Emlen DJ, Pearson DE (2016) Linking native and invader traits explains native spider population responses to plant invasion. PLoS ONE 11:1–17

    Google Scholar 

  • Sol D, Griffin AS, Bartomeus I, Boyce H (2011) Exploring or avoiding novel food resources? The novelty conflict in an invasive bird. PLoS ONE 6:1–7

    Article  Google Scholar 

  • Stamp NE (1978) Breeding birds of riparian woodland in south-central Arizona. Condor 80:64–71

    Article  Google Scholar 

  • Stoleson SH, Shook RS, Finch DM (2000) Breeding biology of Lucy’s warbler in southwestern New Mexico. Western Birds 31:235–242

    Google Scholar 

  • Stromberg J (1998) Dynamics of Fremont cottonwood (Populus fremontii) and saltcedar (Tamarix chinensis) populations along the San Pedro River, Arizona. J Arid Environ 40:133–155

    Article  Google Scholar 

  • Strong TR, Bock CE (1990) Birds species distribution patterns in riparian habitats in southeastern Arizona. Condor 92:866–885

    Article  Google Scholar 

  • Szaro RC (1981) Bird population responses to converting chaparral to grassland and riparian habitats. Southwest Nat 26:251–256

    Article  Google Scholar 

  • R Development Core Team (2010) The R project for statistical computing

  • Tracy JL, Robbins TO (2009) Taxonomic revision of biogeography of the Tamarix-feeding Diorhabda elongata (Brullé, 1832) species group (Coleoptera: Chrysomelidae: Galerucinae: Galerucini) and analysis of their potential in biological control of Tamarisk. Magnolia Press, Florida, pp 1–152

    Google Scholar 

  • Whitmore RC (1977) Habitat partitioning in a community of passerine birds. Wilson Bull 89:253–265

    Google Scholar 

  • Yard HK, van Riper IIIC, Brown BT, Kearsley MJ (2004) Diets of insectivorous birds along the Colorado River in Grand Canyon, Arizona. Condor 106:106–115

    Article  Google Scholar 

  • Zavaleta E (2000) The economic value of controlling an invasive shrub. Ambio 29:462–467

    Article  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge the Landscape Conservation Cooperative and the United States Department of Agriculture (USDA) for their financial support for this project. Comments from two anonymous reviewers substantially improved this paper, we are grateful for their suggestions. We offer our sincerest gratitude to D. N. Rakestraw and Z. D. Watson for their field and lab assistance. We thank Northern Arizona University graduate students including M. C. Rotter, P. J. Motyka, I. D. Eammons, G. C. Cummins, K. E. Ironside, and J. Peiffer for reviewing earlier drafts of this manuscript, and to R. L. Hammond, T. A. Whitham, C.A. Gehring and B. J. Butterfield for their guidance with statistical analyses. This work was supported by Bureau of Reclamation and Arizona State University with Grant numbers R12AC80916 and 13-076.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, USA

    Sean M. Mahoney & Tad C. Theimer

  2. Colorado Plateau Research Station, Northern Arizona University, Flagstaff, AZ, USA

    Matthew J. Johnson

  3. Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, NH, USA

    Jeffrey T. Foster

Authors
  1. Sean M. Mahoney
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tad C. Theimer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew J. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeffrey T. Foster
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sean M. Mahoney.

Appendices

Appendices

Appendix 1

See Table 2.

Table 2 Candidate models for the detection probability using half-normal (hn) and hazard-rate (hr) as key-functions and site and habitat as co-variates
Full size table

Appendix 2

See Table 3.

Table 3 Densities (birds/Ha ± SE) of Lucy’s and yellow warblers in each study site along the Virgin River drainage, in Arizona, Utah and Nevada, USA, based on point counts in June and July of 2013 and 2014 as modeled in program DISTANCE
Full size table

Appendix 3

See Table 4.

Table 4 Frequencies of arthropods (±SE) in the diet and number of unique individual Lucy’s warblers and yellow warblers sampled within each habitat type
Full size table

Appendix 4

See Table 5.

Table 5 Biomass estimates (mg) of arthropods (±SE) in the diet and number of unique individual Lucy’s warblers and yellow warblers sampled within each habitat type
Full size table

Appendix 5

See Table 6.

Table 6 Percentage prey biomass of total biomass estimates of arthropods (±SE) in the diet and number of unique individual Lucy’s warblers and yellow warblers sampled within each habitat type
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mahoney, S.M., Theimer, T.C., Johnson, M.J. et al. Similar dietary but different numerical responses to nonnative tamarisk (Tamarix spp.) by two native warblers. Biol Invasions 19, 1935–1950 (2017). https://doi.org/10.1007/s10530-017-1408-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-017-1408-2

Keywords

Search

Navigation