Simulation studies of Senegalese Grasshopper ecosystem interactions II: the role of egg podpredators and birds

Jørgen Aagaard Axelsena*, Bo Svenning Petersenb, Idrissa Halidou Maigac, Abdoulaye Niassyd,Kemo Badjid, Zakaria Ouambamae, Mette Sønderskova and Christiaan Kooymanf,1

aDepartment of Terrestrial Ecology, National Environmental Research Institute, Vejlsøvej 25, DK-8600, Silkeborg, Denmark;bOrbicon, Ringstedvej 20, DK-4000, Roskilde, Denmark; cDirectorate of Crop Protection, Niamey, Niger, Present address:Danish National Environmental Research Institute, c/o Regional Centre AGRHYMET, Niamey, Niger; dDirectorate of CropProtection (DPV), Dakar, Senegal; eRegional Centre AGRHYMET, Niamey, Niger; fInternational Institute of TropicalAgriculture, 08 B.P. 0932, Tri Postal, Cotonou, Benin

(Received 24 September 2008; final version received 4 November 2008)

We present a simulation study of the role of birds and egg pod predators in the population dynamics of the Senegalesegrasshopper. The model was an energetics-driven ecosystem model that included a natural Sahelian grass, millet,grasshoppers, the egg pod predators bombyliidae and Tenebrionidae, and 24 species of birds that preyon grasshopper nymphs and adults. The model simulated the rain-dependent dynamics and migration along afive-location south–north transect in Niger and Senegal, and the main outputs were the grasshopper pressure on thetransect, measured as accumulated transect grasshopper days, and the density of eggs ready to emerge the followingrainy season. The model was calibrated using observations from transects in Niger (2003, 2004) and Senegal (2004).When input data from Niger 2003 and 2004 were applied, simulated reductions in grasshopper pressure during

the rainy season from egg pod predators and birds, respectively, were within a range of 18–25%, but takentogether the overall reduction in grasshopper pressure ranged between 35 and 37%. Using input from Senegal(2004) the birds accounted for reductions of around 25%.When the impact of the natural enemies was measured in terms of reduction in the density of eggs hatching the

following year, the simulated impact of the egg pod predators ranged between 45 and 83% and that of the birdsbetween 33 and 39%, and the two groups combined caused reductions between 60 and 75%.Analyses of the sensitivity to the bird species, added one by one, showed ‘predator saturation’ along the Niger

transects (with low grasshopper density) but not along the Senegal transect.For Niger, the sensitivity analyses revealed Cattle Egret, Grey-headed Sparrow, Chestnut-bellied Starling,

Bu!alo Weaver, Sudan Golden Sparrow, Grey Hornbill, Red-billed Hornbill and Abyssinian Roller to be themost important individual species. For Senegal the top-five individual bird species were Village Weaver, Bu!aloWeaver, Savile’s Bustard, Grey-headed Sparrow and Abyssinian Roller.

Keywords: simulation model; natural enemies; bird predation; ecosystem modelling; grasshopper control

1. Introduction

The migratory grasshopper Oedaleus senegalensis(Krauss), known as the Senegalese Grasshopper, isa well-known millet pest in the Sahel. It producesthree annual generations, starting during the rains inthe southern Sahel and continuing with the adultsmigrating northwards with the rains as the wet seasonproceeds. There they produce one or two generationsand, as the rainy season comes to an end, the adultsmigrate southwards where they lay diapausing eggsthat remain in the soil during the dry season and giverise to the first generation in the following year(Launois 1978; Launois and Launois-Luong 1989).

Several insect species are predators of grasshoppersin the Sahel, but only a few of these are regarded asparticularly important predators of the SenegaleseGrasshopper. Of importance in relation to predation

of the Senegalese grasshopper are the bombyliid flies ofthe genus Systoechus and the species Xeramoebaoophaga, as well as two genera of beetles, the tenebrionidPimelia senegalensis and the meloid beetles Meloidaespp., all of which are predators of the egg pods in the soil(Greathead et al. 1994). Predation levels on diapausingegg pods of the Senegalese Grasshopper are often veryhigh, levels of between 60 and 100% being common(Colvin 1997; DPV 2003; Maiga 2008). Therefore, it isreasonable to assume that these predators play animportant role in determining the annual populationdynamics of the Senegalese grasshopper.

Most studies dealing with birds as predators ofgrasshopper pests have been conducted in NorthAmerica, while quantitative data from other regions,including sub-Saharan Africa, are very scarce. Severalsmall-scale exclosure experiments in North American

*Corresponding author. Email: jaa@dmu.dk1Present address: Fondation Agir pour l’Education et la Sante, B.P. 6792, Dakar, Senegal.

International Journal of Pest ManagementVol. 55, No. 2, April–June 2009, 99–112

ISSN 0967-0874 print/ISSN 1366-5863 online! 2009 Taylor & FrancisDOI: 10.1080/09670870802617171http://www.informaworld.com

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grasslands indicate that birds may reduce grass-hopper densities by 30–50% at low to medium levelsof infestation, i.e. 1–4 grasshoppers per m2 (e.g. Joern1986, 1992; Fowler et al. 1991; Bock et al. 1992). Athigher grasshopper densities, however, predatione!ects become less important, and overall the roleof avian predation in the dynamics of grasshopperpopulations is variable (Branson 2005). Based onmeasurements and estimates of field metabolic ratesof small passerines, Kirk et al. (1996) estimated that apair of Savannah Sparrow Passerculus sandwichensisand their young would consume 3.7 kg of freshgrasshopper biomass per season. Moreover, potentialgrasshopper predation from the entire grasslandbreeding bird community of Savannah Sparrowduring one season could be as high as 218,000grasshoppers/ha (Kirk et al. 1996).

In northern Nigeria, Anene and Vajime (1990)observed 20 species of birds preying on nymphs andadults of O. senegalensis, and a similar range of avianpredators was reported from Niger by Cheke et al.(1980). However, no quantitative estimates of thepredation and its e!ect on grasshopper densities weremade. Amatobi et al. (1987) studied the e!ect of avianpredation on grasshoppers (mainly O. senegalensis) infallow fields in Nigeria (Kano State), where Cattle EgretBubulcus ibis, Abdim’s Stork Ciconia abdimii andBu!alo Weaver Bubalornis albirostris were the mostimportant predators. Flocks of these species reducedpopulations of grasshopper nymphs in May, at densitiesof 4.6–16.8 nymphs/m2, by 72–82%. When preying onadult grasshoppers (densities 0.5–1.1/m2) in September/October, the birds removed 51–72% of the grass-hoppers. The authors suggest that the large reductionin grasshopper numbers observed was possible becauseof the grasshoppers occurring in pockets, allowing thebirds to converge on these. Hence, similar rates ofremoval are unlikely to occur over larger areas.

The aforementioned work on the importance ofbirds and egg pod predators can provide some data onthe extent to which grasshopper populations are a!ectedby the respective predator type, but how important thesemortality factors are for the seasonal and long-termpopulation dynamics of the Senegalese Grasshopper,which in turn are complicated due to migratorybehaviour of this species, remains unknown. The onlyfeasible way of estimating the importance of naturalenemies for the population dynamics is modelling.Therefore, we present a simulation study of theimpact of insect egg pod predators and avian predatorson the population dynamics of the SenegaleseGrasshopper.

2. Methodology

2.1. The model

The model used for simulating the impact of insectand avian predators was a detailed, physiological-

driven simulation model based on detailed informa-tion on biological characteristics of the importantspecies of the ‘grassland-millet-grasshopper-naturalenemy’ ecosystem in the Sahel. The model operated atthe species level and included: millet, an ‘imaginary’grassland grass (representing the vegetation of thegrassland), the grasshopper pest species Oedaleussenegalensis, a less-damaging grasshopper speciesAcrotylus blondelii (that served as alternative preyfor the egg pod predators), two species of veryimportant egg pod predators (a bombyliid fly and atenebrionid beetle), and 24 species of birds that preyon nympha and adult grasshoppers. The importantevents during the season, such as beginning/end of thegrowing season, sowing of millet, emergence ofgrasshoppers from the soil and migration of O.senegalensis, were all driven by rainfall. The modelwas spatial, including a limited number of locations,in order to take into account the very importantmigration of O. senegalensis from the southern Saheltowards the north (to the pastoral zone at the edge ofthe Sahara desert) during the growing season andback south at the end of the growing season.Furthermore, each location was split into twocompartments, millet fields and grassland, occurringin varying respective proportions. The model hasbeen described in detail by Axelsen (2009) and hasalso been used to assess the e!ects of actualtreatments from 2003 and 2004 in eastern Niger andto establish how to optimize pesticide treatments(Maiga et al. 2009).

2.2. Input to the model

2.2.1. O. senegalensis

Considerable information on the biological charac-teristics of O. senegalensis was available in theliterature (Appendix 1), but a small number ofparameters had to be found by calibration toavailable population density data. The data com-prised two datasets from Niger and one from Senegal.The two datasets from Niger represented low andvery low densities of O. senegalensis, and the datasetfrom Senegal represents very high densities.

2.2.2. Egg pod predators

The egg pod predators included were the tenebrionidbeetle, Pimelia senegalensis, which has been found tobe the most common coleopteran egg pod predator(Van der Valk et al. 1999; Maiga 2008) of O.sengegalensis, and one species of bombyliid flyresembling Xeromoeba oophaga. X. oophaga wasfound to be the most common bombyliid fly in Niger(Maiga 2008).

Some of the input parameters simulating thesetwo species were derived from the literature, somewere taken from closely related species and others

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again were calibrated to simulate a phenology thatwas in agreement with observations from the field andinformation in the literature (Appendices 2 and 3).Initial densities on bombyliid flies came fromobservations in Niger by Maiga (2008), and estimatesof initial densities of tenebrionid were taken from theraw data used by Van der Valk et al. (1999).

The search rate, a problematical parameter inpredator–prey simulations, was found by calibratingthe model to simulate predation percentages thatwere at the same level as those observed in thediapausing egg pods from the Niger transects.Consequently, although not all the biological para-meters of the egg pod predators are species-specific,the predation percentages are realistic in size.

2.2.3. Avian predators

Twenty-four bird species were included in thesimulations: Cattle Egret, Abdim’s Stork, Double-spurred Francolin Francolinus bicalcaratus, Savile’sBustard Eupodotis savilei, Black-headed LapwingVanellus tectus, Senegal Coucal Centropus senegalen-sis, White-throated Bee-eater Merops albicollis, Abys-sinian Roller Coracias abyssinicus, Red-billedHornbill Tockus erythrorhynchus, Grey HornbillTockus nasutus, Singing Bush Lark Mirafra cantil-lans, Chestnut-backed Sparrow Lark Eremopterixleucotis, Black-crowned Sparrow Lark Eremopterixnigriceps, Desert Cisticola Cisticola aridulus, CricketWarbler Spiloptila clamans, Southern Grey ShrikeLanius meridionalis, Piapiac Ptilostomus afer, GreaterBlue-eared Starling Lamprotornis chalybaeus, Long-tailed Glossy Starling Lamprotornis caudatus, Chest-nut-bellied Starling Lamprotornis pulcher, Grey-headed Sparrow Passer griseus, Sudan GoldenSparrow Passer luteus, Bu!alo Weaver and VillageWeaver Ploceus cucullatus.

The selected bird species included all majorgrasshopper-consuming species in the study areas.The selection was based upon estimates of populationdensities and the proportion of diet (including the dietof young) made up of grasshoppers. Populationdensities were calculated from line transect counts(see 2.2.4), while the proportion of diet comprisinggrasshoppers was estimated from information avail-able in the literature (Cramp and Simmons 1977–1994; Fry et al. 1982–2004). The estimates indicatedthat the selected species altogether accounted for inthe region of two-thirds of grasshopper removal byavian predation, while more than 50 species wereresponsible for the remaining third.

Instead of allowing a few selected species torepresent the avian predation, it was decided toinclude a large number of birds in the simulationsbecause the predation is highly variable in nature.Species composition changes dramatically from southto north (Petersen et al. 2007) and also di!ers between

Niger and Senegal. Some bird species prey only onthe largest grasshopper instars, others can only copewith the smallest instars, some have a large propor-tion of grasshoppers in their diet and can almost beregarded as specialists, while others may be regardedgeneralists that to varying degrees switch to grass-hoppers during the rainy season. In some species bothadults and young eat grasshoppers, whereas in otherspecies the adults mainly feed on vegetable matter butraise their young on grasshoppers and other insects.Phenology also di!ers widely among species; somespecies are sedentary and may breed at di!erent timesof the year, some arrive early in the rainy season tobreed while others arrive later in the rainy season,either to breed or after having bred further south.Thus, in order to make a reasonable simulation of therole of birds as natural enemies on the SenegaleseGrasshopper it was deemed necessary to include alarge suite of birds in the simulations. Because thespecies modelled only accounted for approximatelytwo-thirds of the total avian grasshopper consump-tion, their densities were multiplied by 1.5 in thesimulations.

In simulating the interaction between birds andtheir prey (O. senegalensis as well as alternative insectprey) the search rate was calibrated to let the birdssurvive and reproduce with the densities of birds andalternative insect prey observed along the transect in2004. Therefore, the search rates applied wereassumed to give a good description of the ability ofthe birds to search for prey. In order to take otherfood sources into account the food acquired by a birdwas divided by the proportion of its prey that wasestimated to comprise insects. This means that thebirds were assumed to be able to acquire other foodsources with the same e"ciency with which theyacquire insects.

The most important biological characteristics forthe birds involved in the simulations were migrantarrival time, breeding period, estimated percentage ofgrasshoppers in total food consumption, bodyweight, egg weight, clutch size and juvenile develop-ment time (Appendix 4).

2.2.4. Bird counts and density estimation

Bird counts were performed in Niger and Senegal in2003 and 2004, between 7 June and 20 September. Allcounts were carried out during the first four hours ofdaylight, corresponding to the main period of birdactivity. The counts were performed on line transects(Bibby et al. 2000), and each morning’s sessionconsisted of counts on four line transects of 50 minduration. The starting points for the transects wererandomly selected along a road traversing the regionto be censused. The direction of walking was, as arule, west. Intended walking speed while counting was1.2 km/h, and the mean transect length (recorded by

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GPS) was 1058 m. All birds seen or heard on eitherside of the line were identified according to speciesand assigned to one of seven distance bands (0–25,25–50, 50–75, 75–100, 100–200, 200–300, and 300–400 m). Birds seen or heard more than 400 m o! theline were not recorded, nor were birds only seenflying, with the exception of birds in song-flight –these were assigned to the distance band where theywere first discovered. After completing each transect,the observer walked briskly for a further 8–10 min toensure that the transects were independent of eachother. A total of 331 and 276 transects werecompleted in Niger and Senegal, respectively.

Based on the field counts, absolute densities werecalculated for each bird species and transect, usingDistance 4.1 software (Thomas et al. 2003). Thespecies-specific probability of detection was assumednot to di!er significantly between sites, so a commondetection function model was fitted to data from alltransects. Choice of model followed the recommen-dations of Buckland et al. (1993) and was mainlybased upon a low value of Akaike’s InformationCriterion and a good visual fit to the distribution ofrecords. For most species a hazard-rate model fittedthe data well. The computed E!ective Strip Width(ESW, the distance where the number of birdsoverlooked inside the strip equals the numberrecorded outside the strip) varied between 35 and400 m. The estimated densities may, depending onthe species concerned, represent the number ofterritories/advertising males, the number of indivi-duals, or fall somewhere in between. To adjust forthis, estimated densities were converted to populationdensities using a species-specific multiplication factorof between 1 and 1.8. For each species, populationdensities were finally averaged for all transects within0.258 latitude of the grasshopper count sites to give amean density for each site.

2.2.5. Alternative insect prey

No estimates of general insect density in the Sahel,according either to latitude or progress of the rainyseason, were found to exist. Therefore, a 2-weekinvestigation was carried out along the Niger transectin June 2004 at the same time as the bird counts. Themethod was derived from the way grasshopper countsare usually carried out in the Sahel (Popov 1980; Vander Valk et al. 1999). An ‘imaginary quadrat’ wasidentified, and the insects within this quadrat werecounted. First, at a distance, adult grasshoppers andother larger flying insects escaping from the quadratas the person carrying out the survey approachedwere counted. Second, the grasshopper nymphs andother jumping insects were counted when kneelingnext to the imaginary quadrat. Third, small bushesand tufts of grass were searched and finally shakenand the insects were counted as they left. And fourth,

the soil and soil crevices were searched for surface-dwelling insects. Here, counting involved the numberof insects within three size groups: 55, 5–10, and410 mm. Some of the insects were sampled foridentification and sorting into the three sizegroups. The grasshopper count was carried out inquadrats of 2 m2, and other insects were countedin quadrats of 1 m2, both daily, and at the same timeas the ornithological counts. A total of 36 grass-hopper counts were made and 18 counts of otherinsects.

There is a general relationship between insectlength and their dry weight:

DW ! 0:0305L2:62

where DW is dry weight in mg and L is length in mm(Rogers et al. 1976). The three size classes wereconverted from lengths to dry weight, assuming theaverage size of the insects smaller than 5 mm was4 mm, the average size of the 5–10 mm group was7.5 mm and the average size of the above 10-mmgroup was 15 mm.

These data were analysed for relationships be-tween latitude and density without finding goodcorrelations; but a rather good correlation was foundbetween the density of grasshoppers (number ofindividuals/area unit) and the density of alternativeprey (number of individuals/area unit or g/area unit).The relationship between the density of grasshoppersand the density of alternative insect prey was found togive good correlation using the equation:

A ! a" GHb

where A is the density of alternative prey, a and b areconstants and GH is the grasshopper density mea-sured in numbers per area unit. The results constitut-ing the foundation for the constants are shown inTable 1 and the values of the constants are shown inTable 2. The results show a moderate to strongrelationship between the two factors, both whenexpressing the density of alternative prey in numberof individuals and as estimated dry weight; althoughthe correlation is strongest using number of indivi-duals. However, the correlations are strongly sig-nificant in both cases, and the correlation was usedwhen modelling the density of alternative preyavailable for birds in the simulations. In thesesimulations it was assumed that the relationshipremained the same throughout the rainy season. Theassumption of a constant relationship between grass-hopper density and that of alternative prey issupported by the fact that the Sahelian ecosystem israin-driven, and that both grasshoppers and alter-native prey are to a large extent dependent on thissame factor, although the degree of dependency mayvary from species to species.

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2.3. Low density calibration data from Niger

The simulation of O. senegalensis was calibrated byaid of datasets collected in 2003 and 2004 along asouth–north transect in the eastern Niger, south andnorth of the town of Zinder. The transect comprisednine sample locations placed on a migration route ofO. senegalensis from south (13.157168N–9.608628E)to north (15.602808N–7.931348E) in Niger (Maiga2008). The nine locations were selected on the basis ofgrasshopper (especially Oedaleus senegalensis) infes-tations in the last 5 years and the experience ofpersonnel from Niger’s plant protection agency(DPV). National and local o"ces at Niamey andZinder made available these data. The sampling sitesat each location were chosen according to knownhabitat and food preferences of O. senegalensis andsoil type preference for oviposition (Garba 1998;Popov 1980). For simplicity, data from only five ofthese locations were used in the calibration, and theselocations were selected to represent the entire south–north transect.

Density of egg pods was estimated according tothe method described by Popov (1980), and for theestimate of egg density an average of 25 eggs per podwas used (Launois and Launois-Luong 1989). Grass-hopper density estimates were made separately foradults and hoppers (juveniles). The density of adultswas estimated by counting grasshoppers on three1 6 100-m transect lines. The density of hoppers wasestimated by counting the individuals in 25, 1-m2

squares situated on a line in three replicates. Thequadrats were separated by five steps according toVan der Valk et al. (1999).

Rainfall data were collected by Niger’s plantprotection agency’s (DPV) local personnel in smallmeteorological stations equipped with simple rainmeasure jars. The pesticides used by DPV to treatO. senegalensis on the south–north transect werecompounds such as Fenitrothion, Chlorpyrifos andTralomethrine, and actual pesticide applications wereincluded in the calibration.

2.4. High density calibration data from Senegal

The model was calibrated to simulate a dataset of O.senegalensis densities from a transect on the south–north migration route in Senegal consisting of fivesites (Fisker et al. 2007). This dataset came fromcounts of total density (all stages) of O. senegalensisat regular intervals – 4 days for some sites and 7–8days for others – and from collected rainfall data. Thesampling commenced in August, which was duringthe second generation of O. senegalensis. Themethods were the same as those used in Niger, butthere were no data on egg pod predators.

Table 1. The density of grasshoppers and alternative prey (in numbers and estimated dry weight) for birds along the Zindertransect in June 2004.

Date Transect GH meanAlternative insect prey

(mean no/m2)Alternative insect prey

(mean dw/m2)

yymmdd new no. no/m2 55 mm 5–10 mm 410 mm 55 mm 5–10 mm 410 mmTotal/m2 (mg)

Total/ha (g)

040607 401 1.29 4.34 2.24 0.68 0.500 1.340 2.501 4.342 43.418040608 402 0.98 8.42 1.94 0.74 0.971 1.161 2.722 4.853 48.533040609 403/404 1.65 3.88 3.06 2.40 0.447 1.831 8.828 11.106 111.063040610 405/406 1.34 2.56 0.96 0.46 0.295 0.574 1.692 2.562 25.615040611 407/408 0.35 1.68 0.50 0.14 0.194 0.299 0.515 1.008 10.077040612 409/410 0.40 2.42 0.56 0.52 0.279 0.335 1.913 2.527 25.267040613 411/412 1.37 3.30 1.76 0.22 0.380 1.053 0.809 2.243 22.427040614 413/414 0.79 1.96 1.08 0.22 0.226 0.646 0.809 1.681 16.813040615 415/416 0.41 4.28 1.28 0.26 0.493 0.766 0.956 2.216 22.156040616 417/418 0.02 1.62 0.54 0.20 0.187 0.323 0.736 1.246 12.455040617 419/420 2.57 2.18 1.26 1.50 0.251 0.754 5.518 6.523 65.228040618 421/422 5.48 1.12 0.68 0.48 0.129 0.407 1.766 2.302 23.016040619 423/424 2.82 3.00 0.46 0.28 0.346 0.275 1.030 1.651 16.509040620 425/426 0.31 1.08 0.42 0.06 0.125 0.251 0.221 0.596 5.964040621 427/428 1.42 1.68 0.70 0.34 0.194 0.419 1.251 1.863 18.631040622 429/430 0.51 2.98 1.24 0.22 0.343 0.742 0.809 1.895 18.946040623 431/432 0.12 2.80 0.52 0.14 0.323 0.311 0.515 1.149 11.488040624 433/434 0.23 2.02 0.32 0.10 0.233 0.191 0.368 0.792 7.921

Table 2. The correlation analysis results between thedensity of grasshoppers and the density of alternative preyon the Zinder transect in June 2004.

Number/m2

Numbers/ha Mg/m2 g/ha

A 5.568 4005.7 1415.81 1.41581B 0.286 0.286 0.307 0.307Correlation

coe"cient0.71 0.71 0.547 0.547

% Variationexplained

49.7 49.7 29.9 29.9

P value 0.011 0.011 0.018 0.018

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2.5. The calibration procedure

Calibration was performed visually with help fromgraphic representation of the simulated densities incomparison with observed densities. The parameterschanged during calibration to the Niger data were themortality rates of juveniles and adults, the minimumand maximum rainfall per decade and per month thatcontrolled the suitability of the habitat forO. senegalensis, the fraction of the adult populationmigrating when the habitat became unsuitable, andthe timing of the start of the migration from north tosouth.

In calibration to the Senegal data only a fewparameters were changed: the input density of eggsfrom all five locations, the date when the direction ofthe migration switched from north to south, and themortality rates. The parameters relating to the e!ectof rainfall on habitat suitability and migration weretaken from the calibration to the Niger transect. Onthe Senegal transect only 20–30% of the two north-ernmost locations were sprayed and, therefore, theproportion of the population killed by spraying was0.25 in simulation of the population dynamics of thistransect.

Calibration of the model to simulate data fromthe migration routes in Niger and Senegal was not anattempt to simulate real population dynamics andmigration in the field. The simulation model com-prised five even-sized compartments placed in a rowwhere the grasshoppers migrate from one compart-ment to the other. The real field situation is acontinuum of habitats situated along a south–northtransect where the general migration pattern isknown, but at the local scale the migration maywell be towards north-east or north-west. The actualhabitats are very likely not of the same size, whichmeans that at some locations the grasshoppers arediluted on a relatively large area and at others theyare condensed to relatively small suitable areas.Furthermore, in a field situation it cannot be takenfor granted that migrants from Location 1 will land inLocation 2. They may choose another route ormigrate for a shorter or longer distance. Therefore,the model represents a simplification of the realsituation, and calibration of the model to the datawas performed in order to obtain the best possibleestimates for a number of unavailable parameters, thecalibration was not an attempt to simulate real-worlddata.

2.6. Simulations

The calibrated model was used to estimate the roles ofthe two groups of natural enemies in grasshoppercontrol, individually and combined, in terms of boththe grasshopper pressure during the rainy season andthe density of eggs ready to hatch by the start of the

following rainy season. The grasshopper pressure wasmeasured in units of ‘accumulated transect grass-hopper days’, i.e. an accumulation of the dailydensities of all stages of grasshoppers at all fivelocations on the transect. Since the model wascalibrated to produce an egg pod predation level atthe start of the following rainy season of approxi-mately 60% this level is not a model output, but theestimate of the e!ect of the egg pod predators on thegrasshopper pressure during the rainy season is amodel estimate. Furthermore, the model was used tosimulate the impact of the entire suite of bird speciesby including them into the simulations one by one,and to investigate the role of the bird species byrunning simulations with each species separately.

3. Results

The simulations clearly showed that the naturalenemies, i.e. both birds and egg pod predators, playa considerable role in regulation of O. senegalensis. Inthe 2003 simulations along the Niger transects the eggpod predators alone accounted for a reduction of24% in grassland and 19% in millet, and in the 2004simulations they reduced grasshopper pressure by 18and 21% in grassland and millet, respectively. On theother hand, in the 2003 simulations, the birds aloneaccounted for 24 and 25% reductions in grasslandand millet, respectively, and in the 2004 simulationsthe figures were 21 and 20%, respectively. Together,the two groups of predators together accounted for a37% reduction in O. senegalensis in the grassland anda 35% reduction in the millet fields in the 2003simulation; in the 2004 simulations the respectivefigures were 35 and 37% (Figure 1). In the 2004Senegal simulations the birds accounted for areduction of 26% in millet and 25% in grassland,while the role of the egg pod predators was notassessed due to the lack of field data on egg podpredation in this dataset.

To investigate the importance of the naturalcontrol mechanisms in relation to the followingseason, we undertook full-year simulations based onthe density of eggs ready to hatch at the start of thefollowing rainy season. These included the impact ofthe egg pod predation on the diapausing eggs andproduced results somewhat di!erent from those in theone-season simulations. In these simulations thecontrol exerted by the egg pod predators clearlyexceeded the control exerted by the birds. Using the2003 input data the birds reduced the followingseason’s egg input by 35 and 34% in grassland andmillet fields, respectively, while the respective figuresfor egg pod predators alone were 67 and 60%.Combined, the bird and egg pod predators reducedthe grasshopper pressure by 74% in grassland and69% in millet fields (Figure 2). Using the 2004 inputdata avian predation reduced the grasshopper

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pressure by 39 and 33% in grassland and millet,respectively, and egg pod predators by 60 and 82%,respectively. Together, they reduced the density ofeggs ready to emerge the following year in bothgrassland and millet by 65 and 79%, respectively(Figure 2). The lower reduction resulting from birdsand egg pod predators combined was due tocompetition for the resources causing weaker popula-tion development in the two predator groups.

Simulations of the large number of di!erent birdspecies involved in grasshopper control showed thatadding bird species one by one generally improvedgrasshopper control until approx. 15–17 species hadbeen included. This was the case using Niger inputdata from both 2003 and 2004. Adding further speciesto the simulations only slightly improved grasshoppercontrol (Figure 3). The same simulations usingSenegal input data and the species most abundantthere showed that grasshopper control generallyimproved each time a new species was introduced,

and there was no levelling o! tendency as in the Nigersimulations. In order to investigate the individualroles of the various bird species, they were alsointroduced into the simulated ecosystem on anindividual basis. In the Niger simulations CattleEgret was the most important species in 2003 and in2004 the most important species was Grey-headedSparrow followed closely by Cattle Egret. In the 2003simulations Abyssinian Roller, Bu!alo Weaver,Sudan Golden Sparrow, Grey-headed Sparrow,Grey Hornbill and Senegal Coucal were also amongthe top eight. In the 2004 simulations Senegal Coucalwas replaced by Red-billed Hornbill among the topeight species. In the Senegal simulations five specieswere clearly more important than the rest; thesespecies were Village Weaver, Bu!alo Weaver, Savile’sBustard, Grey-headed Sparrow and Abyssinian Roll-er, with the two weavers as the most importantspecies (Figure 4). These rankings of importance werebased both on the densities observed at di!erent

Figure 1. The impact of birds and egg pod predators on the ‘accumulated transect grasshopper days’ (A, C and E) and thereduction expressed in percent (B, D and F) in grassland and millet fields. A and B: Niger 2003 input data, C and D: Niger2004 input data, E and F: Senegal 2004 input data.

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locations (di!erent latitudes) and simulated grass-hopper consumption. In the Niger simulations the eggpod predators were included to make the situation asreal as possible, and in the Senegal simulations therole of other natural enemies was included in back-ground mortality.

4. Discussion

The simulations presented here clearly showed thatthe Senegalese grasshopper was strongly influencedby natural control mechanisms in Niger in 2003 and2004 and in Senegal in 2004. They also revealed somerelatively minor di!erences in grasshopper controlbetween years and geographic locations, despitegrasshopper densities di!ering markedly betweenNiger and Senegal, with much higher densities inSenegal. The results suggest, as in Van der Valk et al.(1999), that where chemical pesticides are applied that

destroy the natural enemies of grasshoppers, e.g. eggpod predators, there is a risk that the pest problemwill be exacerbated.

Our simulations showed that the relative role ofthe two investigated groups of natural enemies, birdsand egg pod predators, depended on how the role wasmeasured. Using density of eggs by the end of the dryseason (instead of accumulated transect grasshopperdays), includes the mortality of diapausing eggsduring the dry season, which appeared to beimportant when looking at the grasshopper problemover the longer term. Also, the importance of thebirds in reducing the number of eggs was almostdouble that of reducing initial grasshopper pressure,even though the birds do not prey on egg pods duringthe dry season. This result was due to the di!erentfocus on the stage of the grasshoppers’ life cyclewithin these two measures – if killed late instars oradults have already contributed considerably to the

Figure 2. The impact of birds and egg pod predators on the average (average of the five locations) density of eggs ready toemerge the following year (A and C) and the reduction expressed in percent (B and D) in grassland and millet fields. A and B:Niger 2003 input data, C and D: Niger 2004 input data.

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accumulation of grasshopper days, but they do notcontribute to the pool of diapausing eggs.

The simulated results obtained on the role of thebirds as biocontrol agents of O. senegalensis (reducingthe grasshopper pressure by between 20 and 25%) area little lower than the observations made in Joern(1986, 1992), Fowler et al. (1991) and Bock et al.(1992), who found that birds reduce grasshopperdensity by 30–50% at low to medium levels ofinfestation in North America. However, the variationpresent in these North American results is consider-able and sometimes it was not even possible todemonstrate the impact of birds (Joern 2000). Bycontrast, our simulated results are all in the range of20–25% and have been obtained at di!erent bird andgrasshopper densities. In the two simulation seriesfrom the Niger transect, the grasshopper density was

clearly higher in 2003 than in 2004, but remained lowboth years. In the simulation series of the Senegal2004 situation, the grasshopper density was at leastone order of magnitude higher, but the simulatedresult was removal of approximately the samepercentage of grasshoppers. These outputs contrastwith the conclusion of Branson (2005) that avianpredation e!ects become less important at highgrasshopper densities. The main reason for therelatively important role of birds in the Senegalsimulations, where the grasshopper densities wererelatively high, was the higher density of birds inSenegal.

Taking the role of natural enemies into considera-tion, it would appear worth considering how theirrole could be increased further, e.g. by increasing thenumber of trees to provide more nesting sites for

Figure 3. The simulated number of ‘accumulated transect grasshopper days’ when the bird species were added one by one tothe simulated ecosystem.

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birds, releasing new introduced (exotic) naturalenemies, augmenting indigenous ones, or reducingpesticide treatments that kill egg pod predators.However, the Niger simulations (2003 and 2004), inwhich bird species were added to the ecosystem modelone by one, indicate that the impact of measures toenhance predation might not necessarily be worth-while (Figure 3); adding birds species beyond around15 species had no or very limited impact on thegrasshopper pressure. On the other hand, a similarsaturation e!ect seemed not to occur when using theinput data from Senegal 2004. The significantdi!erence between the Niger and Senegal simulationsis the density of O. senegalensis, which was muchhigher in Senegal 2004. This suggests that thepresence of more predators would be beneficial at

densities higher than the ones seen in Niger in 2003and 2004, when the potential for improved controldue to a greater number of predators was lostthrough competition among the predators.

Some of the bird species that have been identifiedas most important in grasshopper control may beconsidered surprising because they are not grass-hopper, or even insect, specialists. However, CattleEgret, Abdim’s Stork and Bu!alo Weaver were foundby Amatobi et al. (1987) to be the most importantavian predators on grasshoppers in their study area,and of these Cattle Egret and Bu!alo Weaver werealso included in our top-five. The weavers, VillageWeaver and Bu!alo Weaver are mostly seed-eatersoutside of their breeding season, but switch tograsshoppers and other insects while breeding, and

Figure 4. The simulated reduction in ‘accumulated transect grasshopper days’ when the birds were included one species at atime.

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particularly while feeding their young. Their impor-tance is based on their high abundance and the factthat they are not strongly dependent on grasshoppers,which have the e!ect that they are present in thehabitat and start breeding even at low grasshopperdensities. Therefore, they consume grasshoppers evenat low grasshopper densities early in the rainy season,having a ‘lying-in-wait strategy’ (Murdoch et al.1985), which prevents these grasshoppers from con-tributing to population build-up over the entireseason. A similar e!ect is seen in the control of aphidsin cereals fields in northern Europe where it has beenfound to be important to kill the stem mothers(fundatrices) early in the season. The generalistpredators are present in the habitat at the arrivaltime of the aphids and have the potential to act as veryimportant control agents (Symondson et al. 2002).

5. Conclusions

Egg pod predators were found to be very importantnatural control agents for the Senegalese grass-hopper. Predation from birds was revealed to bealmost as important as that from egg pod predatorsin controlling grasshopper pressure during the rainyseason, but the egg pod predators were moreimportant in controlling the density of eggs ready togive rise to the following season’s grasshopperpopulation. The most important bird species werefound to be highly abundant generalist species whichdo not depend strongly on grasshoppers.

Acknowledgements

This study was financed by the Danish Aid AgencyDANIDA as part of the PRELISS project.

References

Anene C, Vajime C. 1990. Parasites, parasitoids andpredators of Oedaleus senegalensis Krauss (Orthoptera:Acrididae) in Nigeria. Insect Sci Applic. 11(1):27–34.

Amatobi CI, Apeji SA, Oyidi O. 1987. E!ect of someinsectivorous birds on populations of grasshoppers(Orthoptera) in Kano state, Nigeria. Samaru J AgriRes. 5:43–50.

Axelsen J. 2009. Simulation studies of SenegaleseGrasshopper ecosystem interactions I: the ecosystemmodel. J Pest Manag. 55(2):85–97.

Bock CE, Bock JH, Grant MC. 1992. E!ects of birdpredation on grasshopper densities in an Arizonagrassland. Ecology. 73(5):1706–1717.

Bibby CJ, Burgess ND, Hill DA, Mustoe S. 2000. Birdcensus techniques. 2nd ed. London: Academic Press.

Branson DH. 2005. Direct and indirect e!ects of avianpredation on grasshopper communities in northernmixed-grass prairie. Environ Ecol. 34:1114–1121.

Brun G. 1970. Cycle biologique de Pimelia bipunctata (Col.Tenebrionidae) dans les dunes du littoral provencaleet languedocien. Ann Soc Entomol Fr. (N.S.). 6:655–671.

Buckland ST, Anderson DR, Burnham KP, Laake JL.1993. Distance sampling: estimating abundance ofbiological populations. London: Chapman & Hall.

Cheke RA, Fishpool LDC, Forrest GA. 1980. Oedaleussenegalensis Krauss (Orthoptera: Acrididae). An ac-count of the 1977 outbreak in West Africa and notes oneclosion under laboratory conditions. Acrida. 9:107–132.

Colvin J. 1997. Biotic and abiotic factors a!ecting thepopulation dynamics of the Senegalese grasshopper,Oedaleus senegalensis. In: Krall S, Peveling R, BaDiallo, editors. New strategies in locust control. Basel:Birkhauser Verlag. p. 63–67.

Cramp S, Simmons KEL. editors. 1977–1994. The birds ofthe western palearctic. (Vols. I–IX). Oxford: OxfordUniversity Press.

DPV 2003. Annual report from Directorate of PlantProtection. Niger, 2003.

Fisker EN, Bak J, Niassy A. 2007. A simulation modelto evaluate control strategies for the grasshopperOedaleus senegalensis in West Africa. Crop Prot.26:592–601.

Fowler AC, Knight L, George TL. 1991. E!ects of avianpredation on grasshopper populations in North Dakotagrasslands. Ecology. 72(5):1775–1781.

Fry CH, Keith S, Urban EK. editors. 1982–2004. The birdsof Africa. (Vols. I–VII). London: Academic Press.

Garba Y. 1998. Role de l’occupation des sols sur lepeuplement acridien de la region de Banizoumbou(Niamey, Niger). These de doctorat, Universite ParisXI. 219 p.

Gillon Y, Gillon D. 1974. Recherches ecologiques sur unesavane sahelienne du Ferlo septentrional, Senegal:Donnes quantitatives sur les tenebrionides. Terre etVie. 28:296–306.

Greathead DJ. 1958. Observations on two species ofSystoechus (Diptera: Bombyliidae) preying on thedesert locust, Schistocerca gregaria (Forskal) in easternAfrica. Entomophaga, Tome. III:3–22.

Greathead DJ. 1962. A review of the insect enemies ofAcridoidea (Orthoptera). Trans Royal Entomol SocLondon. 114:437–517.

Greathead DJ, Kooyman C, Launois-Luong MH, PopovGB. 1994. Les ennemis naturels des criquets du Sahel.PRIFAS/CIRAD, 147 pp.

Joern A. 1986. Experimental study of avian predationon coexisting grasshopper populations (Orthoptera:Acrididae) in sandhills grasslands. Oikos. 46:243–249.

Joern A. 1992. Variable impact of avian predation ongrasshopper assemblies in sandhills grasslands. Oikos.64:458–463.

Joern A. 2000. What are the consequences of non-linearecological interactions for grasshopper control strate-gies? In: Lockwood JA, Latchininsky AV, Sergeev MG,editors. Grashoppers and grasland health. Managinggrasshopper outbreaks without risking environ-mental disaster). Dordecht: Kluwer Academic Pub-lishers. p. 131–144.

Kirk DA, Evenden MD, Mineau P. 1996. Past and currentattempts to evaluate the role of birds as predators ofinsect pests in temperate agriculture. Curr Ornithol.13:175–269.

Launois M. 1978. Modelisation ecologique et simulationsoperationnelle en acridologie. Application a Oedaleussenegalensis K. Ministere de la cooperation, Paris etGERDAT, Montpellier, France, 212 pp.

Launois M, Launois-Luong MH. 1989. Oedaleus senega-lensis (Krauss, 1877), sautereau ravageur du Sahel.Collection Acridologie Operationnelle, 4, CILSS-DFPV, Niamey, Ministere des A!aires etrangeres desPays-Bas, La Haye, CIRAD, Montpellier.

International Journal of Pest Management 109

Downloaded By: [University of Arizona] At: 00:44 20 November 2010

Maiga IH. 2008. Ecologie du Criquet senegalais Oedaleussenegalensis (Krauss, 1877) en Afrique de l’Ouest etstrategies de lutte. These de doctorat, UniversiteMontpellier 2.

Maiga IH, Axelsen JA, Badji K, Kooyman C. 2009.Simulation studies of Senegalese Grasshopper ecosys-tem interactions III: optimization of grasshoppercontrol. J Pest Manag. 55(2):113–120.

Murdoch WW, Chesson J, Chesson PL. 1985. Biologicalcontrol in therory and practice. Am Nat. 125:344–366.

Petersen BS, Christensen KD, Jensen FP. 2007. Birdpopulation densities along two precipitation gradientsin Senegal and Niger. Malimbus. 29:101–121.

Popov GB. 1980. Studies on oviposition, egg developmentand mortality in Oedaleus senegalensis(Krauss),(Orthoptera, Acridoidea) in the Sahel. Centre forOverseas Pest Rsearch.

Rogers LE, Hinds WT, Buschbom RL. 1976. Generalweight vs. length relationship for insects. Ann EntomolSoc Am. 69:387–389.

Symondson WOC, Sunderland KD, Greenstone MH. 2002.Can generalist predators be e!ective biocontrol agents?Annu Rev Entomol 47:561–594.

Thomas L, Laake JL, Strindberg S, Marques FFC, BishopJ, Buckland ST, Borchers DL, Anderson DR, BurnhamKP, Hedley SL, et al. 2003. Distance 4.1, Release 2.Research Unit for Wildlife Population Assessment,University of St. Andrews, UK.

Van der Valk HCGH, Niassy A, Beye AB. 1999. Doesgrasshopper control create grasshopper problems? –Monitoring side-e!ects of fenitrothion applications inthe western Sahel. Crop Prot. 18:139–149.

Appendix 1. Input data list on O. senegalensis including sources.

Parameter Value and units Source

Optimal temperature 398C Blandford et al. (1998)Optimal development rates:Eggs 6.7%/day Launois and Launois-Luong (1989)Larval stage 1, 2, 3 and 4 33%/day Estimated after Launois and

Launois-Luong (1989)Larval stage 5 25%/dayImmature adults 15%/dayMature adults 3.5%/day Assumeda

Temperature response variation factor 8.9 Estimated after data in Blandfordet al. (1998) and Launois (1978)

Optimal growth rate 0.0133 Estimated after data in Launois andLaunois-Luong (1989)

Mass of egg (DW) 0.625 mg (DW) Launois and Launois-Luong (1989)Mass of adults 128 mg (DW)b Launois and Launois-Luong (1989)Reproduction rate 0.0065 (g/g/%)c

Survival:Eggs and juvenile stages 0.995 (per %)d Calibrated to Niger 2004 data

0.997 Calibrated to Niger 2003 data0.9984 Calibrated to Senega l2004 data

Adults 0.993 Calibrated to Niger 2004 data0.994 Calibrated to Niger 2003 data0.996 Calibrated to Senegal 2004 data

Percentage of laid eggs in diapause before 9/7: 0% Popov (1980)9/7: 14%9/9: 15%9/15: 83%9/20: 97%

after 9/25: 100%Fraction of adults leaving unsuitable habitat pr day 0.092 Calibrated to dataRainfall triggering development after diapause 20 mm Rule of thumb in SahelDecade range of rainfall (pd) making habitat suitable 12 mm 5 pd 5 33 mm Calibrated to 2004 datae

Monthly range of rainfall (pm) making habitat suitable 30 mm 5 pm 5 61 mm Calibrated to 2004 data

aAssumed duration of adult stage 4 weeks.bDW assumed to be 25% of WW. Average for females and males mass used.cg eggs/g female/% development time.dSurvival per % development time.eSlightly modified from values given by Launois (1978).

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Appendix 2. Input data list on bombyliid fly (egg pod predator).

Parameter Value and units Source

Optimal temperature 398C Assumed to follow O. senegalensisOptimal development rates:

Eggs, larval stage 1, 2 and 3 50%/day Eggs # all larval stages: 8 daysGreathead (1958)Pupal stage 5 9%/day

Immature adults 10%/dayMature adults 10%/day

Temperature response variationfactor (L1, L2, L3, L4, L5, young adults, adults)

8.9 Assumed to follow O. senegalensis

Optimal growth rate 0.033 Fitted to suit the mass increase fromegg to adult

Mass of egg (DW) 6.5 E72 mg (DW) Greathead (1962)Mass of adults 30 mg (DW) Weighed in laboratoryReproduction rate 0.25 (g/g/%) Greathead (1962)Survival – all stages 1 No information availableSearch rate (for eggs pods) 0.008 Adjusted to suit the predation rate

observed by Maiga (2008)Percentage of laid eggs in diapause Assumed to follow O. senegalensisEmergence time Fits the emergence of

ovipositing O. senegalensisAdjusted parameter

Appendix 3. Input data list on tenebrionid beetle (egg pod predator).

Parameter Value and units Source

Optimal temperature 408C Brun (1970)Optimal development rates:

Eggs 16.8%/day Fitted to suit observed distribution between larvae and adults in rawdata from Van der Valk et al. (1999)

Larval stage 0.65%/day Brun (1970)Pupae 16%/dayImmature adults 10%/dayMature adults 0.38%/day

Temperature response variationfactor (Eggs, Larvae, Pupae,young adults, adults)

13 Brun (1970)

Optimal growth rate 0.023 Fitted to suit the mass increase from egg to mature larva, Brun (1970)Mass of egg (DW) 4.1 mg (DW) Brun (1970)Mass of adults 375 mg (DW) Gillon and Gillon (1974)Reproduction rate 0.0042 (g/g/%) Parameters chosen to produce a predation rate of the degree of

magnitude observed in Niger 2003 and 2004Survival:Eggs 0.998 (per %)Juvenile stages 0.998 (per %)Adults 0.998 (per %)Search rate 0.008

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Appendix

4.Inputdatalist

forbirds.

Species

Density

(ha7

1)a

May

be

presentin

simulation

from

m/y

b

Breeding

period

(m/y–m

/y)b

Percentage

insects

indietb

Search

rate

cAverage

number

ofeggs/broodsb

Location1

Location2

Location3

Location4

Location5

Abdim

’sStork

0.012

0.0075

0.0045

0.0315

05/1

6/10–9/1

900.01

3AbyssinianRoller

0.282

0.178

0.078

0.0165

0.0275

6/1

7/1–8/30

100

0.01

3Black-crowned

Sparrow-lark

00.003

0.447

1.344

1.698

5/1

6/1–9/30

500.01

2.4

Black-headed

Lap

wing

0.0375

0.012

0.056

0.024

0.006

5/1

6/1–8/1

600.01

2Bu!aloWeaver

0.266

0.138

0.186

0.039

05/15

6/1–9/30

500.01

2.4

CattleEgret

0.009

0.135

0.27

0.41

0.117

5/15

6/15–8/15

750.01

2.6

Chestnut-bellied

Starling

0.237

0.257

0.765

0.293

0.06

5/15

6/1–10/15

700.01

3.5

Chestnut-backed

Sparrow-lark

00.186

0.884

1.38

0.034

5/1

9/1–12/1

600.01

1Cricket

Warbler

0.041

0.282

0.558

0.404

0.654

8/1

8/15–8/30

100

0.01

4DesertCisticola

0.054

0.408

0.446

0.396

0.108

5/1

6/1–9/30

100

0.01

2.4

Greater

Blue-earedStarling

0.008

0.008

0.0285

0.014

0.029

5/15

6/15–8/15

500.01

4Grey-headed

Sparrow

0.912

0.804

0.509

0.15

0.105

5/15

6/15–8/15

500.01

4GreyHornbill

0.435

0.104

0.027

0.0015

06/1

6/15–8/15

600.01

2Long-tailed

GlossyStarling

0.093

00

00

5/15

8/15–9/30

700.01

2.3

Piapiac

0.173

00

00

5/1

6/1–9/30

100

0.01

2.4

Red-billedHornbill

0.405

0.104

0.028

0.003

0.014

6/1

8/1–10/1

900.01

4Senegal

Coucal

0.111

0.012

00

05/1

5/15–10/15

750.01

3SingingBush-lark

0.009

0.135

0.27

0.41

0.117

5/1

9/1–12/1

800.01

1SouthernGreyShrike

0.016

0.166

0.269

0.225

0.233

5/15

6/20–10/15

650.01

4.8

Village

Veawer

0.033

0.02

0.041

0.005

05/15

6/1–10/30

500.01

2.4

White-throated

Bee-eater

00.02

0.042

0.275

0.75

6/1

7/1–8/30

100

0.01

3

aPetersenet

al.(2007).

bFry

etal.(1982–2004).

c Fittedto

lettheobserved

density

ofbirdsraisetheaveragebroodsize.

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