Skip to main content

Advertisement

SpringerLink
Log in

Exotic black rats increase invertebrate Ordinal richness in urban habitat remnants

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

Abstract

Exotic predators have had devastating impacts on native wildlife globally and have stimulated many attempts to control or eradicate them. However, removing an exotic predator is predicted to have wider consequences if the exotic predator plays an apex role in its new community, including negative impacts on other community members via disruption to trophic or ecological cascading processes. Here, we examine the potential role of the commensal black rat (Rattus rattus) as an exotic higher-order predator in urban habitat remnants in Sydney, Australia. Given that black rats are generalist predators on invertebrates that occupy many trophic levels, we applied trophic cascade theory and predicted that there would be an inverse relationship between the numbers of black rats and smaller invertebrate predators, especially spiders, and a positive relationship between black rats and the numbers, richness and diversity of lower-order invertebrates that are preyed upon by spiders. Using a controlled and replicated removal experiment spanning 10 months of rat-removal and 6–12 weeks of invertebrate sampling, we found both more spiders on black rat-removal sites and lower invertebrate Ordinal richness. Our results thus support our hypotheses and suggest that this exotic rodent may suppress spiders but have an overall positive influence on other invertebrates, perhaps by ‘releasing’ them from spider predation. Although further experimental studies are needed to test the generality of our findings and to critically identify the causal processes involved, we conclude that—at least in certain circumstances—an exotic predator can have potentially positive effects on components of its new ecosystem.

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
Fig. 5

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 M, Gorley R, Clarke K (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. The University of Auckland, Auckland

    Google Scholar 

  • Banks PB, Smith HM (2015) The ecological impacts of commensal species: black rats, Rattus rattus, at the urban–bushland interface. Wildl Res 42:86–97

    Google Scholar 

  • Banks PB, Cleary GP, Dickman CR (2011) Sydney’s bubonic plague outbreak 1900–1910: a disaster for foreshore wildlife? Aust Zool 35:1033–1039

    Google Scholar 

  • Barnes MC, Persons MH, Rypstra AL (2002) The effect of predator chemical cue age on antipredator behavior in the wolf spider Pardosa milvina (Araneae: Lycosidae). J Insect Behav 15:269–281

    Google Scholar 

  • Bell TP (2009) A novel technique for monitoring highly cryptic lizard species in forests. Herpetol Conserv Biol 4:415–425

    Google Scholar 

  • Binz H, Bucher R, Entling MH et al (2014) Knowing the risk: crickets distinguish between spider predators of different size and commonness. Ethology 120:99–110

    Google Scholar 

  • Braun-Blanquet J (1932) Plant sociology. The study of plant communities (trans: Fuller GD, Conard HS), 1st edn. McGraw-Hill Book Co., New York, London

  • Broome K, Cox A, Golding C et al (2014) Rat eradication using aerial baiting: current agreed best practice used in New Zealand (Version 3.0). New Zealand Department of Conservation, Wellington, New Zealand

  • Bucher R, Binz H, Menzel F et al (2014) Effects of spider chemotactile cues on arthropod behavior. J Insect Behav 27:567–580

    Google Scholar 

  • Christie FJ, Cassis G, Hochuli DF (2010) Urbanization affects the trophic structure of arboreal arthropod communities. Urban Ecosyst 13:169–180

    Google Scholar 

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

    Google Scholar 

  • Copson G (1986) The diet of the introduced rodents Mus musculus L and Rattus rattus L on sub-Antarctic Macquarie Island. Wildl Res 13:441–445

    Google Scholar 

  • Cox JG, Lima SL (2006) Naiveté and an aquatic–terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680

    PubMed  Google Scholar 

  • Craddock P (1997) The effect of rodent control on invertebrate communities in coastal forest near Auckland. The University of Auckland, New Zealand

    Google Scholar 

  • Daniel M (1973) Seasonal diet of the ship rat (Rattus r. rattus) in lowland forest in New Zealand. Proc N Z Ecol Soc 20:21–30

    Google Scholar 

  • Dickman CR (2007) The complex pest: interaction webs between pests and native species. In: Lunney D, Eby P, Hutchings P, Burgin S (eds) Pest or guest: the zoology of overabundance. Royal Zoological Society of New South Wales, Mosman, pp 208–215

    Google Scholar 

  • Dickman CR (2014) Micro-carnivores: the ecological role of small dasyurid predators in Australia. In: Glen AS, Dickman CR (eds) Carnivores of Australia: past, present and future. CSIRO Publishing, Melbourne, pp 241–262

    Google Scholar 

  • Dickman CR, Newsome TM (2015) Individual hunting behaviour and prey specialisation in the house cat Felis catus: implications for conservation and management. Appl Anim Behav Sci 173:76–87

    Google Scholar 

  • Doherty TS, Glen AS, Nimmo DG et al (2016) Invasive predators and global biodiversity loss. Proc Natl Acad Sci USA 113:11261–11265

    PubMed  PubMed Central  CAS  Google Scholar 

  • Enders F (1975) The influence of hunting manner on prey size, particularly in spiders with long attack distances (Araneidae, Linyphiidae, and Salticidae). Am Nat 109:737–763

    Google Scholar 

  • Estes JA, Palmisano JF (1974) Sea otters: their role in structuring nearshore communities. Science 185:1058–1060

    PubMed  CAS  Google Scholar 

  • Estes JA, Terborgh J, Brashares JS et al (2011) Trophic downgrading of planet earth. Science 333:301–306

    PubMed  CAS  Google Scholar 

  • Fey K, Banks PB, Oksanen L et al (2009) Does removal of an alien predator from small islands in the Baltic Sea induce a trophic cascade? Ecography 32:546–552

    Google Scholar 

  • Foelix R (2010) Biology of spiders. Oxford University Press, Oxford

    Google Scholar 

  • Fukami T, Wardle DA, Bellingham PJ et al (2006) Above-and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol Lett 9:1299–1307

    PubMed  Google Scholar 

  • Gales R (1982) Age-and sex-related differences in diet selection by Rattus rattus on Stewart Island, New Zealand. N Z J Zool 9:463–466

    Google Scholar 

  • Genovesi P (2005) Eradications of invasive alien species in Europe: a review. Issues Bioinvasion Sci 7:127–133

    Google Scholar 

  • Glen AS, Dickman CR, Soulé ME et al (2007) Evaluating the role of the dingo as a trophic regulator in Australian ecosystems. Austral Ecol 32:492–501

    Google Scholar 

  • Gorvett H (1956) Tegumental glands and terrestrial life in woodlice. Proc Zool Soc Lond 126:291–314

    Google Scholar 

  • Green PT (2014) Mammal extinction by introduced infectious disease on Christmas Island (Indian Ocean): the historical context. Aust Zool 37:1–14

    Google Scholar 

  • Hall S (1980) The diets of two coexisting species of Antechinus (Marsupialia: Dasyuridae). Aust Wildl Res 7:365–378

    Google Scholar 

  • Harris DB, Macdonald DW (2007) Interference competition between introduced black rats and endemic Galapagos rice rats. Ecology 88:2330–2344

    PubMed  Google Scholar 

  • Henschel J (1994) Diet and foraging behaviour of huntsman spiders in the Namib dunes (Araneae: Heteropodidae). J Zool 234:239–251

    Google Scholar 

  • Hobbs RJ, Harris JA (2001) Restoration ecology: repairing the earth’s ecosystems in the new millennium. Restor Ecol 9:239–246

    Google Scholar 

  • Howald G, Donlan C, Galván JP et al (2007) Invasive rodent eradication on islands. Conserv Biol 21:1258–1268

    PubMed  Google Scholar 

  • Jackson ST, Hobbs RJ (2009) Ecological restoration in the light of ecological history. Science 325:567–568

    PubMed  CAS  Google Scholar 

  • JMP (2014) JMP version 9.0.0. SAS Institute Inc., Cary, NC, USA

  • Krebs CJ (1966) Demographic changes in fluctuating populations of Microtus californicus. Ecol Monogr 36:239–273

    Google Scholar 

  • Kurle CM, Croll DA, Tershy BR (2008) Introduced rats indirectly change marine rocky intertidal communities from algae-to invertebrate-dominated. Proc Nat Acad Sci USA 105:3800–3804

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kuschel G, Worthy T (1996) Past distribution of large weevils (Coleoptera: Curculionidae) in the South Island, New Zealand, based on Holocene fossil remains. N Z Entomol 19:15–22

    Google Scholar 

  • Lampert A, Hastings A, Grosholz ED et al (2014) Optimal approaches for balancing invasive species eradication and endangered species management. Science 344:1028–1031

    PubMed  CAS  Google Scholar 

  • Levene H (1960) Robust tests for equality of variances. Contributions to probability and statistics: Essays in honor of Harold Hotelling 2:278–292

  • Matthews A, Dickman CR, Major RE (1999) The influence of fragment size and edge on nest predation in urban bushland. Ecography 22:349–356

    Google Scholar 

  • Meadows AJ, Crowder DW, Snyder WE (in press) Are wolves just wasps with teeth? What invertebrates can teach us about mammal top predators. Food Webs. doi:10.1016/j.fooweb.2016.09.004

  • Moran MD, Hurd L (1997) A trophic cascade in a diverse arthropod community caused by a generalist arthropod predator. Oecologia 113:126–132

    PubMed  Google Scholar 

  • Norman FI (1970) Food preferences of an insular population of Rattus rattus. J Zool 162:493–503

    Google Scholar 

  • O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’on an oceanic island. Ecol Lett 6:812–817

    Google Scholar 

  • Oedekoven MA, Joern A (2000) Plant quality and spider predation affects grasshoppers (Acrididae): food-quality-dependent compensatory mortality. Ecology 81:66–77

    Google Scholar 

  • Oliver I, Beattie AJ (1996) Invertebrate morphospecies as surrogates for species: a case study. Conserv Biol 10:99–109

    Google Scholar 

  • Pace ML, Cole JJ, Carpenter SR et al (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488

    PubMed  CAS  Google Scholar 

  • Palmer ME, Pons G (1996) Diversity in western Mediterranean islets: effects of rat presence on a beetle guild. Acta Oecol 17:297–305

    Google Scholar 

  • Paolucci EM, MacIsaac HJ, Ricciardi A (2013) Origin matters: alien consumers inflict greater damage on prey populations than do native consumers. Divers Distrib 19:988–995

    Google Scholar 

  • Pauwels K, Stoks R, De Meester L (2005) Coping with predator stress: interclonal differences in induction of heat-shock proteins in the water flea Daphnia magna. J Evol Biol 18:867–872

    PubMed  CAS  Google Scholar 

  • Payton IJ, Fenner M, Lee WG (2002) Keystone species: the concept and its relevance for conservation management in New Zealand. Department of Conservation, Wellington

    Google Scholar 

  • Persons MH, Walker SE, Rypstra AL et al (2001) Wolf spider predator avoidance tactics and survival in the presence of diet-associated predator cues (Araneae: Lycosidae). Anim Behav 61:43–51

    PubMed  Google Scholar 

  • Pitkänen A, Kouki J, Viiri H et al (2008) Effects of controlled forest burning and intensity of timber harvesting on the occurrence of pine weevils, Hylobius spp., in regeneration areas. Forest Ecol Manag 255:522–529

    Google Scholar 

  • Polis GA, Hurd SD (1995) Extraordinarily high spider densities on islands: flow of energy from the marine to terrestrial food webs and the absence of predation. Proc Natl Acad Sci USA 92:4382–4386

    PubMed  PubMed Central  CAS  Google Scholar 

  • Preisser EL, Bolnick DI (2008a) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLoS ONE 3:e2465

    PubMed  PubMed Central  Google Scholar 

  • Preisser EL, Bolnick DI (2008b) When predators don’t eat their prey: nonconsumptive predator effects on prey dynamics. Ecology 89:2414–2415

    PubMed  Google Scholar 

  • Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509

    Google Scholar 

  • PRIMER (2012) Primer-E and PERMANOVA+ (version 6.0). Primer-E.Ltd, Plymouth, UK

  • Punzo F, Farmer C, Cook J (2006) Life history and ecology of the wolf spider Pardosa sierra Banks (Araneae: Lycosidae) in southeastern Arizona. Southwest Nat 51:310–319

    Google Scholar 

  • Raubenheimer D, Simpson S (1993) The geometry of compensatory feeding in the locust. Anim Behav 45:953–964

    Google Scholar 

  • Řezáč M, Pekár S, Lubin Y (2008) How oniscophagous spiders overcome woodlouse armour. J Zool 275:64–71

    Google Scholar 

  • Ripple WJ, Beschta RL (2012) Trophic cascades in Yellowstone: The first 15 years after wolf reintroduction. Biol Conserv 145:205–213

    Google Scholar 

  • Ripple WJ, Larsen EJ, Renkin RA et al (2001) Trophic cascades among wolves, elk and aspen on Yellowstone National Park’s northern range. Biol Conserv 102:227–234

    Google Scholar 

  • Ripple WJ, Estes JA, Beschta RL et al (2014) Status and ecological effects of the world’s largest carnivores. Science 343:151–162

    CAS  Google Scholar 

  • Ritzmann RE (1984) The cockroach escape response. In: Eaton RC (ed) Neural mechanisms of startle behavior. Springer, New York, pp 93–131

    Google Scholar 

  • Rovero F, Hughes RN, Chelazzi G (1999) Cardiac and behavioural responses of mussels to risk of predation by dogwhelks. Anim Behav 58:707–714

    PubMed  CAS  Google Scholar 

  • Ruscoe WA, Sweetapple PJ, Perry M et al (2013) Effects of spatially extensive control of invasive rats on abundance of native Invertebrates in mainland New Zealand forests. Conserv Biol 27:74–82

    PubMed  Google Scholar 

  • Salo P, Korpimäki E, Banks PB et al (2007) Alien predators are more dangerous than native predators to prey populations. Proc R Soc Lond Ser B Biol Sci 274:1237–1243

    Google Scholar 

  • Scarff F, Rhind S, Bradley J (1998) Diet and foraging behaviour of brush-tailed phascogales (Phascogale tapoatafa) in the jarrah forest of south-western Australia. Wildl Res 25:511–526

    Google Scholar 

  • Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399

    Google Scholar 

  • Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153

    PubMed  Google Scholar 

  • Shapira I (2012) Behavioural ecology of New Zealand invasive rodents (Rattus norvegicus and Mus musculus): implications for rodent control. Massey University, Aukland

    Google Scholar 

  • Silliman BR, Bertness MD (2002) A trophic cascade regulates salt marsh primary production. Proc Nat Acad Sci USA 99:10500–10505

    PubMed  PubMed Central  CAS  Google Scholar 

  • Simberloff D, Martin J-L, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66

    PubMed  Google Scholar 

  • Simpson S, Raubenheimer D (1993) A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philos Trans R Soc Lond Ser B Biol Sci 342:381–402

    Google Scholar 

  • Sinclair A, Pech RP (1996) Density dependence, stochasticity, compensation and predator regulation. Oikos 75:164–173

    Google Scholar 

  • Sinclair L, McCartney J, Godfrey J et al (2005) How did invertebrates respond to eradication of rats from Kapiti Island, New Zealand? N Z J Zool 32:293–315

    Google Scholar 

  • Smith K, Acevedo-Whitehouse K, Pedersen A (2009) The role of infectious diseases in biological conservation. Anim Conserv 12:1–12

    Google Scholar 

  • Smith HM, Dickman CR, Banks PB (2016) Nest predation by commensal rodents in urban bushland remnants. PLoS ONE 11:e156180

    Google Scholar 

  • Smith HM, Dickman CR, Banks PB (in press) Using effect size benchmarks to assess when alien impacts are actually alien. Sci Rep

  • St Clair JJH (2011) The impacts of invasive rodents on island invertebrates. Biol Conserv 144:68–81

    Google Scholar 

  • Sweetapple P, Nugent G (2011) Chew-track-cards: a multiple-species small mammal detection device. N Z J Ecol 35:153–162

    Google Scholar 

  • Terborgh J, Estes JA (2010) Trophic cascades: predators, prey, and the changing dynamics of nature. Island Press, Washington

    Google Scholar 

  • Towns DR, Simberloff D, Atkinson IA (1997) Restoration of New Zealand islands: redressing the effects of introduced species. Pac Conserv Biol 3:99–124

    Google Scholar 

  • Towns DR, Wardle DA, Mulder CP et al (2009) Predation of seabirds by invasive rats: multiple indirect consequences for invertebrate communities. Oikos 118:420–430

    Google Scholar 

  • Tuomisto H (2010) A consistent terminology for quantifying species diversity? Yes, it does exist. Oecologia 164:853–860

    PubMed  Google Scholar 

  • Undheim EA, King GF (2011) On the venom system of centipedes (Chilopoda), a neglected group of venomous animals. Toxicon 57:512–524

    PubMed  CAS  Google Scholar 

  • Watts C, Thornburrow D (2009) Where have all the weta gone? Results after two decades of transferring a threatened New Zealand giant weta, Deinacrida mahoenui. J Insect Conserv 13:287–295

    Google Scholar 

  • Williams RL, Singleton GR, Dickman CR (2003) The role of interspecific competition in determining macrohabitat use by the black rat and brown rat at Bradley’s Head, NSW. ACIAR Monogr Ser 96:366–370

    Google Scholar 

  • Wyatt KB, Campos PF, Gilbert MTP et al (2008) Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease. PLoS ONE 3:e3602

    PubMed  PubMed Central  Google Scholar 

  • Yang S, Liu Z, Xiao Y et al (2012) Chemical punch packed in venoms makes centipedes excellent predators. Mol Cell Proteom 11:640–650

    CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by an Australian Research Council Grant (LP100100600). Thanks to all field and lab volunteers for assistance in data collection. Also thanks to the Banks Lab at Sydney University for helpful comments on the manuscript.

Funding

This work was funded by an Australian Research Council grant (LP100100600).

Author information

Authors and Affiliations

  1. School of Life and Environmental Sciences, The University of Sydney, The Cottage (A10), Science Road, Sydney, NSW, 2006, Australia

    Helen M. Smith & Peter B. Banks

  2. School of Life and Environmental Sciences, The University of Sydney, Room 321, Heydon-Laurence Building (A08), Sydney, NSW, 2006, Australia

    Chris R. Dickman

Authors
  1. Helen M. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chris R. Dickman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter B. Banks
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Helen M. Smith.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This work was conducted under Scientific License No. SL100174 from the NSW National Parks and Wildlife Service, with Animal Care and Ethics approval from The University of Sydney (L04/6-2011/3/5549). All experimental protocols were carried out in accordance with the approved methods.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig S1

Linear regression of the percentage of chew track cards (CTCs) attacked by rats as a function of black rat density. Each point represents a separate 1-ha bushland site in urban Sydney in which black rat abundance was assessed by trapping (EPS 6 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Smith, H.M., Dickman, C.R. & Banks, P.B. Exotic black rats increase invertebrate Ordinal richness in urban habitat remnants. Biol Invasions 19, 1315–1328 (2017). https://doi.org/10.1007/s10530-016-1340-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-016-1340-x

Keywords

Search

Navigation