349 and c,d Most of the new alien populations appear in large 16 – 13 , 7 where they may not only cause damage in parks, gardens Monk parakeets were trapped on a massive scale for export 17 12 Correspondence to: J-LResearch Postigo, Team, Biogeography, Department of Diversity Animaldad and Biology, de Málaga, Faculty Conservation E-29071 of Malaga, Sciences, Spain. Universi- E-mail: [email protected] Biogeography, Diversity and Conservation Research Team, Departmentmal of Biology, Ani- Faculty of Sciences, Universidad de Málaga, Malaga, Spain Faculty of Architecture and Town Planning, Technion –nology, Haifa, Israeli Israel Institute of Tech- Evolutionary Ecology Group, University of Antwerp, Antwerp, Belgium Terrestrial Ecology Unit, Ghent University, Ghent, Belgium Departamento de Botànica, FacultadBurjassot, de Valencia, Farmacia, Spain Universidad de Valencia, ∗ c a e d b year. to other countries as pets, andpopulations worldwide there owing is to intentional a releases growing or number accidental escapes. of new and orchards but can also damage human infrastructure (e.g. by cities, Diederik Strubbe Par- b in Israel. Is it time to 6 – Boddaert, are native to South America but have established populations 4 Myiopsitta 9 , 8 The most out- 7 , 3 a,e However, alien birds are fre- Assaf Shwartz, Myiopsitta monachus 3 – 1 a* Scopoli, and the monk parakeet, : 349–353 www.soci.org © 2016 Society of Chemical Industry Both species are known to be able to cause . It is unique among parrots in that it builds a 73 11 , 10 2017; growth rate; invasive parrot; Israel; population dynamics; range expansion Boddaert

Psittacula krameri

The monk parakeet is a highly social and vociferous parrot that extensive agricultural damage in their native ranges. is capable ofSouth acting America. as a pest species in its natural range of Pest Manag Sci Informationonthedistributionandpopulationgrowthofinva- sive alien speciesthe can early be stages of difficulttypically the to occur invasion at obtain, process, low when especially densities. invading during species 1 INTRODUCTION sound the alarm? Abstract BACKGROUND: Monk parakeets, Jose-Luis Postigo, Myiopsitta monachus (wileyonlinelibrary.com) DOI 10.1002/ps.4349 Unrelenting spread of the alien monk parakeet Research Article Received: 21 December 2015 Revised: 28 June 2016 Accepted article published: 1 July 2016 Published online in Wiley Online Library: 12 August 2016 Keywords: Supporting information may be found in the online version of this article. in North America, Europe, Africa and Asia.stick They are nests claimed may to damage act as human agricultural infrastructure.Basin pests Although and in several their temperate native monk Europe, range, parakeet little and populations their empiricalimpact. communal are data We present are in investigated available the on the Mediterranean theirpotential temporal population impact and size on and spatial agriculture. growth, dynamics distribution and of potential monk parakeets inRESULTS: Monk Israel parakeet to populations assess are theirIsraeli population growing invasion of success exponentially monk and at parakeetsand comprises a shifted approximately higher from 1500 predominantly individuals. rate urban The than areas distribution to that of agricultural the reported landscapes. species elsewhere. hasCONCLUSIONS: The increased In current Israel, monkareas. parakeet populations At are present, growing reportsurgently fast needed of and before agricultural the have population damage dispersed becomesbe are rapidly too implemented. large from scarce. and cities A widespread to to© complete allow 2016 agricultural assessment Society for of cost-effective of Chemical mitigation Industry possible campaigns to management strategies is standing alien species of the Psittacidae arekeet, the ring-necked para- monachus communal nest, which containsthat a are variable used number for of breeding chambers and also for roosting throughout the rots are well-known, widespread andsome charismatic of alien them are birds, considered but to bemay pests also in their cause native damage range and in non-native habitats. quently attractive to humans and conspicuous,their and consequently introduction history has oftenmented. been There (reasonably) is well a docu- generally goodbirds historical worldwide, record of and introduced tributed thus to a avian better understanding invasions of biological invasions. have strongly con- Antonio-Román Muñoz , rt e t et al. N = : 349–353 1 + t 73 N is the population 2017; t N is the intrinsic rate of 1, r + t Pest Manag Sci Population trends for the period We counted the number of nests 24 24 software program. Spatially explicit GIS © is the time interval. palms), monk parakeets normally build t 34) including 67 chambers, where visibil- = n Phoenix we used the number of nests detected in the 30 is the population size at time During the breeding period, breeding pairs defend the 1 29 + , e is the natural logarithm base, t t 1) as a dependent variable and the interaction between N + From across the current Israeli distribution range, we selected In order to determine whether the monk parakeet popula- To explore the differences in population growth rates between individual nests around themerge base and of form a the ring. leavesalways counted For until as this one they reason, nest, finally even nests if in they palm had not trees yet were merged. a number of nests ( ity allowed extensive and detailedactivity, to monitoring estimate chamber of occupancy. We monk conducted the parakeet survey in March before the breeding period to determine totalsize. population Monk parakeets reach sexual maturityyear in (around their 50% third calendar offledging). birds breed for the first time 2 years after population growth and tion growth rates differed betweenassigned urban nests and to rural three habitats, habitatof we classes farmland according in to the theical vicinity amount data of on the invasive nests. monkown Given parakeet the observations, home lack ranges, we of basednests considered empir- on to a be our the distance regular feedingextreme of distance, feeding (RFD) distance 1 and km (EFD). 2 Monk km from parakeets toto were be inhabit the considered the three habitats: agricultural habitats, whenincluded farmland was in their RFD;was semi-agricultural habitats, included when in farmland theirwhen EFD no farmland but was not includedcurves in in were their their fitted EFD. RFD; separately Population urbanthree for growth habitats, habitats. monk parakeets We living usedpotentially in the at these risk RFD of andpotential monk EFD damage, parakeet we to crop calculated the estimate damage. farmlandcentred As the area on a within the area a proxy location circle of of eachnest reported (1998, (2004–2007 2000) or and recorded 2015).using the These QGIS 2.8.3 calculations Wien were performed nest and prevent non-breeders fromthe roosting occupancy inside. survey Therefore, if is conductedtion at size this could time, be the seriously total underestimated. popula- ing The parakeets number per of chamber was roost- estimated by countingof the number birds moving in andremaining in out the and nest at calculating night. The theground, survey number was using conducted binoculars of from between the those 1 htion before of sunset to activity the in cessa- the colony. trees (typically data on land useAuthority. was obtained from the Israeli Nature and Park the three habitats, wenests built a linear model with log(number of period 1998–2015 to estimate monktrends. parakeet population The growth rate of populationthe growth census (r) was data obtained to by the fitting model using the equation at time and the number of chambers,relation even between though these there is parameters arect that indicator strong of can population cor- size. be used as an indi- where 1998–2015 were determinedinformation using was available the about the number number of ofduring chambers the per nests, first nest years as (i.e. 1998, no 2000) theythe were number observed. of We used chambers and estimatesthe of monk occupancy parakeet population to in estimate 2015. 2.3 Data analysis Following thePruett-Jones, methodology proposed by Van Bael and 20 , 19 Breed- www.soci.org J-L Postigo They are 23 18 such as the 21 © 2016 Society of Chemical Industry This is a feasible 27 – 25 Monk parakeets were first The same methodology for 22 In the case of nests in palm 24 We recorded the geographical 28 , 27 , 13 26 Once they are established in cities, urban colonies can act as propagules forrural their areas. spread Evidence to fromcapacity suburban the for United and spread States neighbouring outside suggestswith that urbanised climate their and areas may may be be limited associated to warmer areas, detecting nests was usedcensuses, in birdwatchers, each researchers, zookeepers survey. and Before government and conducting non-governmental the officials were asked via onlinemailing bird forums, lists andpossible websites about the to presence of provide monkthen parakeets as visited in all their much areas. the We informationand reported identify as locations nests to by confirm locating their calling birds. presence wileyonlinelibrary.com/journal/ps 2METHODS 2.1 Study area The study area comprised two locationscoastal in the plain, Israeli low-altitude whereTel-Aviv District the and Central District. parakeets Thesehuman areas were have population the densities first highest in introduced:inhabitants the per country, the square with kilometre 7784 respectively, and andof hold 1527 the over 40% total populationtral of District comprise Israel. urban Thefarmland land Tel-Aviv (6 (87 District and and and 26% 46% Cen- respectively). respectively) and building their bulky communal nests on utility poles). also sometimes perceived as a new source of noise pollution. Mediterranean Basin where food is availableand all year during in large cities partpopulation of estimates the are essential yearabout to in the draw agricultural population definiteguide land. conclusions dynamics management planning. of In Therefore, we an any assessedpopulation the invasive case, current size species of andpopulation monk and to parakeets range dynamics in ofdecades. We Israel the also species determined and over its population the analysedand growth last rate agricultural the two in areas. urban Finally,agricultural areas we potentially exposed identified to damage. and estimated the coordinates and the nestingnest. substrate Damaged (i.e. chambers were tree considered species) towere be of not abandoned each and taken intorepair account their because nests monk continually. parakeets use and detected in 1995 in Yarkon Park,and which is is located the in the largest northern park part in of Israel the Tel-Aviv District. and efficient method to locate colonies,are noisy because and monk conspicuous birds parakeets that spend ain large amount the of time vicinity of their nests. 2.2 Population estimatesMonk and distribution parakeet population censusesthe number were of nests, based number of onof chambers per surveys ‘occupancy’ nest of (i.e. and estimates theHistorical number survey of data birdstions inhabiting were of a available birdwatchers chamber). and fromAuthority officials anecdotal of (Shwartz the observa- A, Israelinests unpublished). Nature and and Five chambers Park systematic wereand surveys conducted of 2015 in prior theApril period to in 2004–2007 the the Mediterranean breeding Basin. season, which starts around ing monk parakeets were first recorded in 1998lished). (Shwartz A, Although unpub- the initial population sizeis in unknown, the four Tel-Aviv birds District were releasedtral in District the in mid-1990s the in same the area Cen- zofe where O, nests private were communication, first 2004). observed (Hat-

350 351 In M. Fur- 21 34 A recent population This infor- 15 32 and so envi- 35 we suggest that 38 M.monachus In Chicago (IL), monk para- 36 wileyonlinelibrary.com/journal/ps which is precisely the type of crop 33 0.303 versus 0.119 respectively). The species is more likely to become extinct = 37 r but also because there is no evidence that they 39 Population growth (1998–2015): population growth of during the period 1998-2015; the labels represent the number Population growth according to habitat: In Israel, the monk parakeet population growth is exponential, Alien monk parakeets are thought to pose a relatively minor monachus of chambers in every year (2004–2015). in colder and less densely populated invaded areas. growth rates according to habitat. Figure 2. Furthermore, since their introductionhave not in only Israel, expanded monk theirtural distribution parakeets areas from but cities alsocolonies to in established agricul- the a vicinity of growing farmland. number of breeding as in other non-native areas,sic but rate it of is population noteworthy growthtimes that in higher the the than intrin- Israeli the populationthe reported is United rate States about ( for 3 alien monk parakeets in Figure 1. the temperate Mediterranean climate may facilitateductive higher and/or repro- survival rates among monk parakeets. threat to agriculture not only becausepogenic of food their reliance on anthro- keets are completely dependent onthe anthropogenic winter foods months. during mation should be considered to be aincrease warning of and future range population expansion, and probablywith of farmers in increased agricultural conflict land. Israelof produced sunflower about 5000 seeds tons in 2014, study showed that monkurban parakeets habitats in are cold areas unlikely ofmismatch to the between United spread States the from owing locations to of climate origin and introduction. that is targeted by the monk parakeet in its native range. ronmental conditions in the invaded area could explain thesuccess relative of monk parakeets in Israel. thermore, climate has been commonly considered tofactor be a that primary affects the distribution of alien species, Israel, however, monk parakeetsstraints do of not surviving face and breeding theto at the energetic cold case of con- temperatures. ringed-necked Similarly parakeets in Israel, 31 M. 0.88), = 2 )of0.303 r R Eucalyptus 2.24). There ± in 2015. How- 2 0.03, = Pinus halepensis C. SM. (4.3%), fan P spp. (16.8%), Phoenix 0.65), whereas in 2015 there were Pinus canariensis in 2015. Thus, there was a significant ± 2 0.421 respectively; in 2004 to about 20.7 km 1.3 monk parakeets per chamber (range = 2 r 0.87) (supporting information Fig. S1). ± spp. (2.0%), and one unidentified species : 349–353 © 2016 Society of Chemical Industry = 2 73 R 2017; 0.962) (Fig. 1). In 2015, 1213 chambers were detected. 0.003, = 0.207 versus 0.489) (Fig. 2). The population doubling times were 1.5, = in 2004 to 72.3 km 2 78.5%). P 2 = R Washingtonia = > r r Urban populations grew more slowly than agricultural popula- was an average of 1.3 3.2 Spatiotemporal patternsAccording of to monk parakeet RFD distribution and EFD, innests 2015 (18.0%) there in were urban 92 habitat, monkand 326 parakeet (63.8%) 93 in (18.2%) agricultural habitat inurban semi-agricultural nests (87) habitat. were The locatedthe in majority Israeli Yarkon Central of District, Park only (Tel six the Aviv monk parakeet District).in nests urban were In habitat, found whereas the rest (413) were locatedand in semi-agricultural agricultural habitats. tions ( 1–6), which corresponded to anconfidence estimated interval 1162–1943) average of monk 1556 parakeets (95% in 2015. palms, of tree (0.2%).majority The tree of species monkEucalyptus differed parakeet trees (59.8%), between followed nests by Aleppo habitats; pines in and date(30.4 the palms urban and areas 9.8% wereagricultural respectively), areas built the whereas in vast in majoritypines ( of semi-agricultural nests and were built in Aleppo between 1 and 20 chambers per nest (average 2.37 3.1 and 1.7 years in semi-agricultural,tats urban and respectively. agricultural Based habi- onincreased the from RFD, 0.58 km the area of farmland at risk (65.9%), followed by date palms, spp. (10.8%), Canary pines, 3.3 Nest substrate In 2015, monk parakeet nests weremajority of found the in nests were five built tree in Aleppo species. pines, The Pest Manag Sci 4 DISCUSSION Since its introduction in Israellation in has 1995, undergone the striking monkrent growth. parakeet population We popu- is estimate about 1500 that individuals, and thepopulation therefore is cur- the the Israeli second largest in EuropeBasin and after the the Mediterranean Spanish population of around 20 000 individuals. 3RESULTS 3.1 Monk parakeetMonk population size parakeet and trends nest censusesexponentially showed in that Israel in the the period population 1998-2015 grew at a rate ( (model Spread of the alien monk parakeet in Israelyear and habitatexplanatory variables. (urban, We tested semi-agriculture modelity assumptions and and for normal- agriculture) non-constant errorBreusch–Pagan as in tests respectively. variance We used usingwhether a Shapiro–Wilk linear the model amount and to of test home ranges agricultural increased land over time. within monk parakeet www.soci.org During the 2004–2007 period, there werebers between 1 per and nest 4 cham- (average 2.23 while there was notions difference in in either growth habitat ratestions between compared ( popula- with semi-agricultural popula- increase in agricultural land at riskperiod of ( crop damage over the study ever, when based on the EFD,1.66 the km farmland at risk increased from et al. Science : 349–353 Wilson Bull , ed. by Sim- 73 : 10–18 (2009). 45 2017; 46 J Appl Ecol Avian Invasions: the Ecology and :835–847 (2006). :391–402 (1994). Pest Manag Sci 43 :195–197 (2001). with regard to alien birds, a com- 19 46 414 Oxford University Press, Oxford, UK (2009). et al. :405–408 (2004). J Appl Ecol Encyclopedia of Biological Invaions Nature 271 , Unraveling the life history of successful invaders. J Biosci (New Delhi, India) :580–583 (2012). :413–424 (1992). et al. Evolution of Exotic Birds. 337 J berloff D and RejmánekUK, M. pp. 404–409 University of (2011). California Press, London, in introduced birds. pathways in an era of globalization. patterns of introduction effort andProc R establishment Soc success Lond B in birds. biological invasions. ductivity of monk104 parakeets in Cordoba, Argentina. tive. As suggested by Strubbe 6 Sol D, Maspons J, Vall-Llosera M, Bartomeus I, García-Peña GE, Piñol 4 Blackburn TM and Duncan RP, Determinants of establishment success 5 Blackburn T, Lockwood J and Cassey P, 1 Hulme PE, Trade, transport and trouble: managing invasive species 7 Cassey P, Blackburn TM, Sol D, Duncan RP and Lockwood JL, Global 2 Hulme PE, Beyond control: wider implications for the3 management of Crook JA, Lag times, in 8 Navarro JL, Martella MB and Bucher EH, Breeding season and pro- 9 Dhindsa MS and Saini HK, Agricultural ornithology: an Indian perspec- may be prudent to followment the precautionary rapid-action principle eradication and campaigns imple- tocurrently prevent being damage, undertaken as in thekeets are United captured Kingdom, and taken where to zoological para- vate parks communication, (Robertson 2015). P,pri- However, prior to implementingcampaigns, such we would recommend conductingof a the feasibility current study situationinvasions that into takes account, including different a cost-benefit aspects analysis, anment of assess- of biological the feasibilityfor of consulting and the engaging public measures opinion, given proposed that monkkeets and para- are a often positively strategy regarded by the citizens. SUPPORTING INFORMATION Supporting information may be found inarticle. the online version of this REFERENCES ACKNOWLEDGEMENTS The authors wouldY like Malihi, to A acknowledgePark Kaplan the Authority. and help We O provided alsoCOST Hatzofe by acknowledge European from Cooperation the in the supportES1304) Science Israeli provided for and Nature the by Technology development (Action and ofmanuscript this are article. the The authors’ contentsany responsibility person of acting and on this its neither behalf is COST responsiblebe for nor the made use of that might the information containedthe in it. people We who are shared indebted information toparakeet all about colonies; the without locations their of contribution monk impossible it to would assess have the been currentIsrael. population Antonio-Román Muñoz of was monk partially supported parakeet byde in the la Juan Cierva programme ofMinistry the of Spanish Agriculture, MEC Food and andPark’s Network by Environment, (project the Spanish 1098/2014). Spanish National prehensive study would be essential to identify theate most appropri- long-term management policiesway and to the manage most the cost-effective agricultural risk ecosystems. posed If by no monkhave parakeets action become in is severe, urban taken the and effort untilbe needed the too large to problems to reduce be damage practically could implemented. its and and 12 8 L., 7% 20 www.soci.org J-L Postigo Dyospiros suburban Pyrus com- 31 , 30 © 2016 Society of Chemical Industry Solanum lycopersicum we advocate that, especially in L. and 37% for pears is taken into account, and also L., 9–36% for different varieties 32 31 , M., 17% for persimmons 30 even though agroecosystems are prone Zea mays The potential impact on crops could be 29 and also studies related to diet and feeding 32 , spp., which is common behaviour in its native 32 20 Prunus domestica However, our study shows that, in contrast to other et al. 40 Cydonia oblonga Very recently, the Agriculture Damage Section of the Triticum such as Israel and other parts of the Mediterranean Basin. Further studies could investigate the effect of land use 41 44 , L. 42 43 L. f., 28% for corn In their native range, and especially in the Argentinian pampa However, the need for a more rigorous evaluation of possi- The potential risk of monk parakeet crop damage needs to kaki invaded areas, monk parakeetsurban strongholds in to agricultural Israel areas have in asimilar spread short situation period from occurred of in time. their A Spain, wherefrom monk Barcelona parakeets to spread farmlands outside theto city different and crops caused (0.4% damage for tomatoes for quinces munis range. Israeli Nature andcation, Park 2015) Authority reported (Kaplan theon A, first wheat flock private of communi- monk parakeets feeding habits as importantnon-native aspects areas. of the biology of this species in wileyonlinelibrary.com/journal/ps travel great distances, agricultural areas, cautious mitigation actionsmented be in urgently order imple- to reducesion population rates. growth Such and range actionsprevent expan- them can from include hatching, or the capturingfeasible. monk sterilisation parakeets Environmental of where agencies eggsconflicts should to in take a action responsibleculture to and manner other reduce and social monitor impactsaction to ecological, is establish needed. agri- whether In and countrieslished, where which or the species where is only not small yet estab- localised populations are present, it to invasions. If the rapid increasethe in United population States size in and invaded Spain areas such as changes and crop rotationin on agricultural the land. expansion of monk parakeets grasslands, monk parakeetsconversion have of natural strongly grasslands benefitedhave to also crops from benefited and from the urban thewhich areas. introduction they commonly They of breed both eucalyptus in South trees, America andareas in in invaded assessed by identifying anddetermining quantifying whether food they resources arerelation and to consumed their by availability. in a selective way in ble monk parakeet impacts andpreclude mitigation rapid strategies management should not actions,short-term especially monk in parakeet Israel, damageConflicts between to where farmers and crops parakeets, if is not managedare properly, not likely unexpected. to result inparakeets (unplanned, (e.g. unauthorised) through cullings poisoning), of risking monk sequences indirect on negative the con- environment. Buildingfrom on monk the parakeet expertise management gained programmes suchcarried as out the in ones the United States, and agricultural habitats, it is reasonable toparakeet assume population that will the continue monk to spreadThis and possibility increase is in also supported Israel. by its nearly omnivorous diet, of round plums the generally favourable environmentalhost conditions area. in Given these the aspects, Israeli highly important susceptible farmland to areas invasion by may the be monk parakeet. be assessed in Israelspecies and is firmly other established. Mediterranean Suchpopulation areas an viability where assessment analyses should the following include Pruett-Jones Conroy and Senar the fact that this parakeet can easily adapt to urban, capacity to build its own nests, its large reproductive output

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