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Animal Behaviour 86 (2013) 651e657

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Animal Behaviour

journal homepage: www.elsevier .com/locate/anbehav

Oosorption and migratory strategy of the milkweed bug, Oncopeltusfasciatus

Alfredo Attisano a,*, Tom Tregenza a, Allen J. Moore a,b, Patricia J. Moore c,*

aUniversity of Exeter, Centre for Ecology and Conservation, Cornwall Campus, Penryn, U.K.bUniversity of Georgia, Department of Genetics, Athens, U.S.A.cUniversity of Georgia, Department of Entomology, Athens, U.S.A.

a r t i c l e i n f o

Article history:Received 17 April 2013Initial acceptance 15 May 2013Final acceptance 21 June 2013Available online 8 August 2013MS. number: 13-00337R

Keywords:conditional strategyflight millinsect reproductive physiologymilkweed bugOncopeltus fasciatusoosorptionpartial migrationphenotypic plasticity

* Correspondence and present addresses: P. J. MooreUniversity of Georgia, 413 Biological Sciences BuildiU.S.A. and A. Attisano, Department of Zoology, UniveStreet, Cambridge CB2 3EJ, U.K.

E-mail addresses: aa770@cam.ac.uk (A. A(P. J. Moore).

0003-3472/$38.00 � 2013 The Association for the Stuhttp://dx.doi.org/10.1016/j.anbehav.2013.07.013

Migration evolves as a response to seasonally unfavourable environments but plasticity in reproductivephysiology is another avenue by which insects can respond to resource-poor conditions. We investigatedthe relationship between individual variation in migratory propensity and the level of response to poorconditions modulated by the female reproductive physiology. We tested the hypothesis that, comparedto migrants, residential behaviour is associated with a higher degree of phenotypic plasticity inoosorption, an adaptive physiological mechanism that allows females to recoup resources from unde-veloped oocytes. Reallocation from reproduction to survival would allow females to skip migration andto cope with unfavourable environments. If this plasticity is evolved, we further predicted it would varybetween as well as within populations. We examined variation associated with migratory behaviour infemales from four populations of the milkweed bug, Oncopeltus fasciatus, using a behavioural assay tocategorize females as either migrant or resident and observing the differences in oosorption betweenthese groups. As expected, food availability, source population and wing length influenced the propensityfor migratory flight, and food availability influenced levels of oosorption. We also found support for ourkey prediction that resident females are characterized by higher levels of ovarian oosorption thanmigrant females. Our study provides support for a physiological difference between migrant and residentfemales and suggests the presence of both physiological and behavioural tactics that interact with thepotential for migration to provide adaptation to seasonally challenging environments.� 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Migration is a complex behavioural syndrome that evolves inresponse to temporal fluctuations in resource availability (Dingle1996; Alerstam et al. 2003). Polymorphism in migratory tendencyis a widespread phenomenon (Chapman et al. 2011); partiallymigratory strategies can occur as a response to ecological condi-tions (e.g. Lundberg 1985; Ball et al. 2001; Hebblewhite & Merrill2009; Boyle 2011; Cagnacci et al. 2011; Mysterud et al. 2011; Skovet al. 2011) or be genetically determined (Biebach 1983; Berthold1991; Pulido 2011). To date, the physiological mechanisms under-pinning individual variation in migratory tendency have beenstudied in only a handful of avian species (Schwabl et al. 1984;Boyle et al. 2010; Nilsson et al. 2011).

, Department of Entomology,ng, Athens 30602-2603, GA,rsity of Cambridge, Downing

ttisano), pjmoore@uga.edu

dy of Animal Behaviour. Published

Much of the partial migration literature has focused on verte-brate species, leaving a large gap regarding invertebrate examples,particularly insects (Chapman et al. 2011). Migration in insects istypically viewed from the perspective of the oogenesiseflightsyndrome (Johnson 1969) which involves a trade-off betweenmigratory ability and reproductive maturation (Dingle 1996; Zera &Denno 1997; Roff & Gélinas 2003). In challenging environments,individuals can either allocate resources to flight and foregoreproduction in favour of survival until new resources have beenfound or allocate current limited resources to reproduction at theexpense of survival and future reproductive potential (Roff &Gélinas 2003). In some insect species variation in migratorybehaviour is manifested in morphological polymorphism witheither the presence or absence of wings or variation in wing lengthinfluencing whether or not individuals migrate (Harrison 1980;Roff & Fairbairn 1991). However, morphological variation is notrequired for variation in migratory behaviour (Dingle 1968; Cooter1982; McAnelly & Rankin 1986).

The link between migration and reproduction suggests thatoocyte resorption (oosorption) could be a mechanism influencing

by Elsevier Ltd. All rights reserved.

A. Attisano et al. / Animal Behaviour 86 (2013) 651e657652

migratory tendency in insects. Oosorption in insects is a physio-logical response to unfavourable environments (Bell & Bohm 1975)in which females resorb nutrients from developing oocytes,investing resources in survival rather than reproduction (Boggs &Ross 1993; Ohgushi 1996). Social factors (Moore & Sharma 2005;Barrett et al. 2009), food availability and starvation (Kotaki 2003;Osawa 2005; Kajita & Evans 2009; Park et al. 2009) and parasiticloads (Hopwood et al. 2001) all influence the level of oosorption.Thus, there is a link between poor environmental conditions andoosorption, which may suggest the presence of a potential alter-native tactic to migration.

Oncopeltus fasciatus is distributed from the Caribbean to south-ern areas of Canada (Feir 1974). It commonly feeds on milkweeds(Asclepias sp.) but can feed on alternative hosts such as Neriumoleander in areas where milkweed plants are temporarily unavai-lable (Klausner et al. 1980; Miller & Dingle 1982). Each year, migra-tory individuals moving from southern overwintering areascolonize northern areas of the U.S. (Dingle 1972, 1996). Differentpopulations showgeographical variation in flight behaviour; highlymigrant bugs from northern areas and sedentary bugs from tropicalareas of Mexico and Caribbean represent the two extremes, whilebugs in the southernU.S. (e.g. Florida andGeorgia) fall somewhere inthe middle in terms of both geography and migratory tendency(Dingle et al. 1980a). Individuals from Iowa show the greatest ten-dency to perform long-distance flight and exhibit a migratory syn-drome in which traits such as wing length, fecundity, developmenttime and flight duration are genetically correlated (Palmer & Dingle1986, 1989). The Puerto Rico population shows the lowest pro-pensity tofly longdistances and traits such aswing length, fecundityand flight duration are not genetically correlated, suggesting theabsence of a similar migratory syndrome (Dingle & Evans 1987;Dingle et al. 1988). However, only a proportion of bugs from north-ern populations perform long-distance flight (Dingle et al. 1980a),and these are either individuals that can perform long-durationflights on consecutive days or individuals that fly just once (Dingle1966). Neither wing muscle histolysis nor brachyptery is involvedin the behavioural polymorphism observed in O. fasciatus (Klausneret al. 1981; Dingle 1996). The lack of morphological differencessuggests there may be physiological differences that characterizedifferent migratory strategies. We have previously shown that thepresence of suboptimal food and starvation increase the amount ofoosorption through apoptosis in females compared to an optimaldiet, allowing them to shift available resources to survival ratherthan reproduction (Moore & Attisano 2011). Thus, this model rep-resents an ideal candidate to address thequestion of howoosorptionmight be related to migratory polymorphism.

We studied females from four populations of O. fasciatus char-acterized by different migratory tendencies (Dingle et al. 1980a) toexamine differences both within and between populations inmigratory tendency and oosorption. We examined the effects ofpopulation, wing length and food availability on the proportion ofvirgin females exhibiting migratory-type behaviour using a flightbehavioural assay to divide females into migratory or residentcategories. We then tested the hypothesis that resident andmigrant females differed in the level of ovarian apoptosis. Our hy-pothesis was that females that are exposed to poor nutritionalconditions could respond either behaviourally, by migrating to anew food source, or physiologically, by resorbing eggs and waitinguntil conditions improve to reproduce. Our second hypothesis wasthat this is an evolutionary adaptation, and therefore the plasticityin this response will depend on the population from which thefemale has been derived. Hence we predicted that migratory pop-ulations would show a lower tendency to use apoptosis to reallo-cate resources from reproduction to survival than residentpopulations.

METHODS

Collection and Rearing

Four populations of milkweed bugs were obtained fromdifferent locations in the U.S.A.: Puerto Rico, Florida, Kentucky andIowa. Apart from Kentucky bugs, all individuals were collected inAugust 2011. The collection period was chosen to maximize sam-pling from populations formed mainly by migrant or resident in-dividuals based on the assumption that during the summer theentire U.S.A. population is divided into migratory northern pop-ulations and residential southern populations (Dingle 1972, 1996).Kentucky bugs were collected in the University of Kentucky Arbo-retum, Lexington, KY in September 2009 from Asclepias syriaca (C.Fox, personal communication). Puerto Rico bugs were collectedfrom Calotropis procera in pasture sites in the southern area of theisland near Santa Isabel. Florida bugs were collected in Homestead,south Florida, from N. oleander, Calotropis gigantea, and fromAsclepias curassavica and Asclepias tuberosa from a plant nursery.Iowa bugs were collected in eastern, central and western Iowa fromA. syriaca and Asclepias verticillata.

In the laboratory, all populations were reared in 14:10 h light:-dark, 25 �C and relative humidity ranging from 50% to 65% and fedon A. syriaca seeds (Educational Science, League City, TX, U.S.A.) andad libitum deionized water for four or five generations before thebeginning of the experiment. Kentucky bugs had been reared in thesame conditions since October 2009. The longer rearing period ofKentucky bugs did not affect their ability to perform migratoryflights, confirming observations on the Iowa population by Dingle(1966).

Only female bugs were used for the experiment, given the na-ture of the ovarian physiological response we wanted to measure.Females are also more likely to fly than males (Dingle 1966). Newlyeclosed adult females were collected daily from nymph coloniesreared at 14:10 h light:dark and 25 �C. Focal females were placed insmall square plastic boxes (110 � 110 mm and 30 mm high) withA. syriaca seeds and a dental wick wettedwith deionized water. Thedental wick was rewetted daily. Focal females were placed in13:11 h light:dark and 24 �C. Density was controlled at five femalesper box. The rearing conditions were chosen to prevent femalesfrom entering diapause (Dingle et al. 1980b).

Females were maintained in these rearing conditions for 6 days.At 7 days of age each female was randomly placed in a petri dish(90 � 15 mm) and assigned to one of the experimental food avail-ability treatments: food present or food removed. Food presentfemales had ad libitum deionized water and milkweed seedsavailable for the entire duration of the experiment while foodremoved females had only deionized water. The amount of food inthe food present treatment was not measured, but seeds wereprovided in enough quantity to sustain individuals for the entireduration of the experiment.

Flight Behaviour

We were first interested in the factors of food availability andsource population and the covariate of wing length underlyingflight behaviour. Based on previous data, we predicted that bothfactors would increase the proportion of females flying and thatpropensity to fly would be greater with longer wing length. Fe-males were flight tested at 8 and 14 days of age using a custom-built tethered flight mill. The ages tested were chosen based onprevious observations about the emergence of the flight responsein milkweed bugs (Dingle 1966). Flight tests were performedfollowing a standardized procedure. A female was attached to anentomological pin using Bostik Blu-Tack. Once secured to the pin,

A. Attisano et al. / Animal Behaviour 86 (2013) 651e657 653

the bug was lifted and stimulated to fly with a puff of air directed tothe head. Usually bugs flew immediately after stimulation, but insome cases they needed to be gently waved in the air to stimulate aflight response. Each female was tested in this way for threeconsecutive times. If in at least one of these tests the flight waslonger than 5e10 s, the pinwas inserted into the flight mill’s arm torecord the flight. Otherwise the bug was categorized as a nonflyer.Bugs that performed a flight burst of at least 10 s during thestimulation trials were likely to fly when attached to the mill’s arm,while bugs that gave a flight burst for less than 5 s never flew oncetethered. Bugs that werewilling to fly responded readily tominimalstimulation, and the experimental manipulations such as liftingand waving the bug or inserting the pin in the mill’s arm did notstop their flight. Thus the preflight stimulation consistentlydistinguished between flying and nonflying bugs. Females that didnot fly were tested again 1 h after the first stimulation to verify thereliability of the first response. In all cases, bugs that did notrespond to the first stimulation did not fly on the same day, even iftested twice. Flight tests were performed at 25 � 1 �C.

Based on previous work by Dingle (1968) and Dingle et al.(1980a), we characterized individual migratory tendency as eithermigrant or resident based on the propensity to engage in a sus-tained and continuous flight occurring before the onset of sexualmaturation. However, while Dingle et al. (1980a) used the totaltime of flight over five trials, we used 1 h of persistent and unin-terrupted flight as our criterion for migratory flight. We found thatindividuals flying continuously for 1 h were likely to fly for verylong periods ranging from 2 to 10 h of uninterrupted flight. In ourexperience, this criterion was a more reliable indicator for migra-tory flight than 30 min total flight time (Dingle et al. 1980a). Fe-males that flew for more than 1 h in at least one of the flight testswere designated as migrants while females that never flew weredesignated as residents. In total 645 bugs were flight-tested and343 classed as migrants (Table 1). Forty-two females flew but forless than 1 h in either or both flight tests and these females werenot considered asmigratory in our analysis. On day 15 females werekilled at �80 �C for 30 min, the right forewing of each focal femalewas collected andwing length, as a proxy for body size (Dingle et al.1980a), was obtained by measuring the longest distance from theaxillary to the apex areas passing through the conjunction betweenradial andmedian veins that approximately marks the centre of thewing. Wing length is highly correlated with weight at eclosion(Dingle et al. 1980a).

Ovarian Apoptosis Assay

Once females were classed as either migratory or resident, weexamined whether they differed in levels of oosorption underalternative food availability conditions. On day 15 from adultemergence a random subset of migratory and resident females

Table 1Sample sizes of the females used for the migratory behaviour assay

Puerto Rico Florida Kentucky Iowa Total

Food present 90 60 85 88 323Food removed 90 59 85 88 322Food present, 1 h flight 42 17 58 38 155Food removed, 1 h flight 60 32 59 37 188Food present, <1 h flight 10 3 1 3 17Food removed, <1 h flight 6 5 7 7 25Food present, no flight 38 40 26 47 151Food removed, no flight 24 22 19 44 109

Based on the result of two flight tests, only females that flew for at least 1 h in atleast one of the flight tests were classed as migrants. Females that flew less than 1 h(N ¼ 42) and females that never flew (N ¼ 260) were classed as residents.

from each population was dissected to assess the level of ovarianapoptosis (Table 2). It has been previously shown that oocyteresorption in O. fasciatus under nutritional stress occurs throughapoptosis (Moore & Attisano 2011).

Ovaries were dissected into phosphate-buffered saline andstained with the Vybrant Apoptosis Assay Kit no. 4 (MolecularProbes, Invitrogen, Eugene, OR, U.S.A.) as described by Moore &Sharma (2005). The kit contains two dyes: the YO-PRO1 can enterapoptotic but not healthy cells giving a green fluorescence, whilethe propidium iodide can enter only cells that are either necrotic orin the late stages of apoptosis giving a red fluorescence(Willingham 1999; Moore & Sharma 2005). Thus healthy cellsremain unstained, while apoptotic oocytes show green fluores-cence and oocytes in late stages of apoptosis or necrosis show redfluorescence. The ovaries were observed using an Olympus BX61epifluorescence microscope (Olympus UK Ltd., London, U.K.).Ovaries of O. fasciatus females are formed by seven ovarioles each.We did not use ovarioles showing tissue damaged during dissec-tion. Therefore the data collected were the total number of ovari-oles showing evidence of apoptosis through green or redfluorescence out of the total number of ovarioles collected intact foreach female. Prior to the dissection a volunteer unaware of thepopulation, treatment and flight response was chosen to code eachfemale randomly. Thus staining and observation were done blindlyin relation to population, treatment and flight behaviour. Codeswere only revealed after scoring the staining levels of the ovaries.

Statistical Analysis

Our first test examined the factors associated with migratorytendency. We used logistic regression to examine the effect ofpopulation, food availability and their interaction on migratorytendency. Wing length was included as a covariate. We used aPearson chi-square test for the comparisons of migratory pro-pensity for each population between food regimes and of migratorypropensity between source populations within food regimes.ANOVA was used for the comparisons of wing length betweenmigrant and resident females within each population. Our secondtest examined the factors associated with oosorption assayed bythe extent of ovarian apoptosis. Our oosorption values werebounded data, that is, proportions were obtained through the countof ovarioles in apoptosis. We transformed the apoptosis data usingan arcsine-square-root transformation and fitted a generalizedlinear model (GLM) with normal distribution to analyse the effectof migratory tendency, population, food availability and all in-teractions on levels of ovarian apoptosis. Wing length was againincluded as a covariate. We used a Wilcoxon chi-square nonpara-metric test for the comparison of levels of oosorption betweenmigratory propensity and within food regimes of pooled females. APearson chi-square test was used for the pairwise comparison oflevel of oosorption between migrant and resident females withineach source population. All analyses were performed using JMP8.0.2 (SAS Institute Inc., Cary, NC, U.S.A.).

RESULTS

Variation in Migratory Tendency

Food availability, source population, and wing length all hadsignificant effects on the migratory tendency of females (Table 3).Fed females in all populations were in general less likely to engagein migratory flight than starved females (Table 3, Fig. 1). However,there was a significant difference between treatments only inFlorida (chi-square test: c2

1 ¼ 4:13, P ¼ 0.042) and Puerto Rico(chi-square test: c2

1 ¼ 8:66, P ¼ 0.003) while there was no

0.45

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0.75

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igra

nts

Table 2Sample size of the females’ subset used for the oosorption analysis and pairwise comparisons for the levels of oosorption between migrant and resident individuals withinpopulation

Food present c2 df P Food removed c2 df P

Migrant Resident Migrant Resident

FL 16 24 0.02 1 0.954 27 14 2.43 1 0.119IA 26 23 4.64 1 0.031 24 22 0.88 1 0.348KY 23 21 0.64 1 0.424 24 22 0.44 1 0.508PR 22 23 9.94 1 0.002 23 22 1.15 1 0.284

FL ¼ Florida, IA ¼ Iowa, KY ¼ Kentucky, PR ¼ Puerto Rico.

A. Attisano et al. / Animal Behaviour 86 (2013) 651e657654

difference between treatments in Iowa (chi-square test: c21 ¼ 0:14,

P ¼ 0.706) and Kentucky (chi-square test: c21 ¼ 0:03, P ¼ 0.865).

Populations also differed in their propensity to undertake migra-tory flights (Table 3, Fig. 1) and there was no interaction betweenfood availability and population (Table 3). In the food presenttreatment Kentucky females had a greater propensity for migratoryflight compared to the other populations (chi-square test:c23 ¼ 17:452, P < 0.001) while there was no difference between

Iowa, Florida and Puerto Rico females (chi-square test: c22 ¼ 2:938,

P ¼ 0.230). In the food removed treatment Iowa females had alower propensity for migratory flight compared to the other pop-ulations (chi-square test: c2

3 ¼ 17:984, P < 0.001) while there wasno difference between Kentucky, Florida and Puerto Rico females(chi-square test: c2

2 ¼ 3:845, P ¼ 0.146). Wing length also had asignificant effect on flight behaviour with larger females morelikely to exhibit migratory flight (Table 3). Migrant females werebigger than residents in Florida (ANOVA: F1,105 ¼ 5.425, P ¼ 0.022),Kentucky (ANOVA: F1,155 ¼ 7.119, P ¼ 0.008) and Puerto Rico(ANOVA: F1,174 ¼ 7.186, P ¼ 0.008) populations, while migrant andresident females were not significantly different in the Iowa pop-ulation (ANOVA: F1,159 ¼ 0.899, P ¼ 0.344; Fig. 2).

Levels of Ovarian Apoptosis

Migratory tendency, food availability and population all hadstatistically significant effects on levels of ovarian apoptosis(Table 4). In addition there was a significant interaction betweenpopulation and treatment but no other interactions were signifi-cant. Wing length was not a significant covariate.

The pattern of the effects of these factors can be seen in Fig. 3. Asexpected, food availability had a significant effect on oosorption,with less food resulting in more ovarian apoptosis (Table 4) in allpopulations. Populations differed in their oosorption response(Table 4). A significant interaction between source population andfood availability suggested that populations differed in theirresponse to food regimes (Table 4). When females from all sourcepopulations were pooled, resident females had higher levels ofoosorption in both the food present (Wilcoxon rank sum test:c21 ¼ 8:77, P ¼ 0.003) and food removed (Wilcoxon rank sum test:

c21 ¼ 5:193, P ¼ 0.023) treatments. However, in the pairwise

comparisons between migrant and resident females, only Iowa andPuerto Rico females in the food present treatment were signifi-cantly different, while all other comparisons were not (Table 2,Fig. 3).

Table 3Factors affecting the variation in migratory tendency

Explanatory variable df c2 P

Population 3 48.04 <0.001Wing length 1 19.17 <0.001Food availability 1 5.19 0.022Food availability*population 3 5.70 0.127

DISCUSSION

Migratory and oosorption strategies have typically been exam-ined independently but our results show that both operate in ourpopulations of O. fasciatus. All females seemed able to performsome level of oosorption plastically in both food regimes, but not allfemales undertook migratory flights, suggesting that the ability tomigrate may be dependent on individual status. However, thevariation in response among populations suggests that there areadaptive differences in adopting these alternative tactics. Theseresults are particularly interesting when considered in the light ofthe individual variation giving rise to patterns of partial migration:which aspects of individual state and which ecological conditionsdetermine who migrates and who remains resident?

Behavioural Variation in Migratory Tendency

Food availability, source population and wing length all affectedthe propensity for migratory flight and all source populationscontained females that demonstrated migratory-type behaviour.Based on previous work by Dingle et al. (1980a) we expected dif-ferences in migratory tendency between the four populations andwhile we found that populations varied, our results differed fromthose previously reported for this species. In general, all

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FloridaIowaKentuckyPuerto Rico

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Figure 1. Migratory tendency, measured as at least 1 h of continuous flight, inresponse to food availability.

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Figure 2. Wing length (mm) �SE, used as a proxy for body size, of migrant andresident females from source populations. Numbers in columns represent sample sizes.*P < 0.05; **P < 0.01.

A. Attisano et al. / Animal Behaviour 86 (2013) 651e657 655

populations showed a higher percentage of fliers than thatobserved by Dingle et al. (1980a). This difference could be caused bythe use of flight mills rather than the static tethering used in earlierstudies. Flight mills may provide more appropriate cues such asmovement through the air to maintain a sustained flight response.Another important difference between our study and the study byDingle et al. (1980a) is that we used virgin females in our trials.Virginity might increase the number of migrating females becauseit affects the trade-off between searching for a new habitat andwaiting to reproduce. The most unexpected result was that we didnot detect a ‘residential’ population with low migratory levels aspreviously reported by Dingle et al. (1980a). Migratory flight ininsects is characterized by its persistent and continuous nature andlack of responsiveness to other stimuli (Kennedy 1961; Dingle1996), not the overall time spent in flight or distance achieved.While our experimental set-up makes it difficult to differentiatebetween long-distance dispersive flight and migratory flight, ourobservations that individuals that flew for 1 h were likely to fly formany hours and that these individuals did not stop flying, evenwhen manually stimulated to do so (A. Attisano, personal obser-vation), convinced us that we were able to distinguish betweenresident and migrant females.

Table 4Factors affecting the variation in levels of oosorption

Explanatory variable df c2 P

Migratory tendency 1 15.20 <0.001Food availability 1 65.58 <0.001Population 3 32.45 <0.001Food availability*population 3 10.67 0.014Food availability*migratory tendency 1 0.51 0.477Migratory tendency*population 3 4.68 0.197Migratory tendency*food availability*population 3 3.47 0.325Wing length 1 0.02 0.877

The behavioural response to food stress showed a more ex-pected pattern, and is consistent with an increase in migratoryactivity as a response to poor food conditions.While all populationscontained a proportion of migratory individuals, this proportionincreased in response to food deprivation only in the southernpopulations of Florida and Puerto Rico. In Iowa populations ofO. fasciatus, starvation is likely to increase the number of short-duration foraging flights, but not the long-duration migratoryones (Dingle 1968). Our results are consistent with this observation.Milkweed plants, the seeds of which represent the main source offood for developing nymphs of O. fasciatus (Chaplin & Chaplin1981), are scattered and rare in southern Florida during summer(Miller & Dingle 1982). In Puerto Rico, milkweed is locally common,but patchy (Dingle 1992). In contrast, milkweed is abundant in Iowaand Kentucky during the summer. Thus host availability is differentbetween northern and southern areas and the flight response in thefood removed regime suggests that southern populations maymigrate in response to cues such as food availability, while northernpopulations may rely mainly on cues such as temperature andphotoperiod. Thusmigration in this species may not be a distinctivefeature only of northern populations, but might happen in southernpopulations as well as a response to the unpredictable distributionof resources.

Which Tactic Should a Female Adopt?

Both the selection pressure on individuals to migrate whenconditions deteriorate (Southwood 1962; Denno et al. 2001;Alerstam et al. 2003; Dingle & Drake 2007) and the physiologicalmechanisms underlying the transition to migratory behaviour(Rankin & Rankin 1980; Rankin & Burchsted 1992; Dingle 1996;Dingle & Winchell 1997; Paez et al. 2011) have been discussed insome detail. In this and in earlier studies of flight behaviour, indi-vidual O. fasciatus can be divided into two distinct categories, flyersand nonflyers, and this variation has been explained as geneticdifferences between populations, environmental stimuli or poordetection power of the experimental procedure (Dingle 1966;Rankin & Riddiford 1977; Dingle et al. 1980a). Our aim, however,is to understand the alternatives to migration available to residentindividuals. We found that all females can respond to challengingconditions by means of physiological plasticity in oosorption inwhich resources are conserved and reallocated until conditionsimprove. However, resident females generally have higher levels ofoosorption than migratory females.

Given the two tactics that we have identified, either reallocateresources and wait or move to a new habitat, what determines thetactic an individual female should use? The ‘decision’ to migrate orremain resident could be a result of a conditional strategy; all fe-males may be capable of both tactics and migrate or remain resi-dent depending on individual state, such as size at maturity. As hasbeen observed previously, body size in O. fasciatus varies betweenpopulations and bigger size seems to be related to migratory pro-pensity (Dingle et al. 1980a). Larger individuals expend relativelyless energy in flight than smaller individuals (Roff & Fairbairn1991), and may be in better physiological condition enablingthem to afford the costs involved in migration (Rankin & Burchsted1992). Smaller females may not have the resources required toundertake a migratory flight and thus must adopt an alternativetactic to cope with the absence of food.

It has previously been shown that in O. fasciatus oosorption is aplastic physiological response to poor nutritional environments(Moore & Attisano 2011). Such a response could allow resident fe-males to cope with suboptimal sources or even total lack of food,leading to the evolution of physiological mechanisms to cope withsuboptimal conditions. Diapause has also been hypothesized as

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Figure 3. Levels of ovarian apoptosis �SE for females from the source populations divided as migrants or residents in (a) food present and (b) food removed conditions. *P < 0.05;**P < 0.01.

A. Attisano et al. / Animal Behaviour 86 (2013) 651e657656

such a mechanism (Klausner et al. 1980). However, our experi-mental conditions were set to avoid entry into diapause and it isunlikely that diapause explains our results.

The tactic adopted by a female could also be the result of geneticdifferences between populations. Northern populations ofO. fasciatus show a ‘migratory syndrome’ with genetic correlationsamong body size, wing length, flight capacity and early fecundity(Palmer & Dingle 1986, 1989), while these correlations are not pre-sent in the tropical Puerto Rico population (Dingle & Evans 1987;Dingle et al. 1988). Our results suggest the possibility of a ‘nonmi-gratory syndrome’ in which another set of genetic correlations maybe associatedwith the ability to perform oosorption, which increasethe ability to survive in a limited food environment or to skipmigration completely by adopting an alternative residential tactic.While we have not undertaken this type of study in O. fasciatus,Edvardsson et al. (2009) showed that the level of ovarian apoptosisunder stressful conditions is heritable in a cockroach.

Conclusion

Regardless of whether the partial migration strategy is condi-tional or solely genetic, our results show that individuals differ intheir propensity to respond both behaviourally and physiologicallyto environmental stimuli. Populations reared under common gar-den conditions still differ in this propensity, suggesting it canevolve. This variation plays a role in determining whether an in-dividual will move to an alternative habitat or remain in the samearea utilizing a tactic that involves physiological accommodation tocope with challenging environments. Our study illustrates the po-tential benefits of investigating basic physiological processes inorder to understand the mechanisms driving the evolution ofpartial migratory strategies. It will be interesting to examine insectmodel species in the context of partial migration given the hugerelevance of insects in the movement of biomass and the growingimportance of this topic in the field of movement ecology. Otherinvertebrates (Hinsch 1992), amphibians (Lehman 1977), reptiles(Bonnet et al. 2008) and fishes (Lubzens et al. 2010) are able toresorb oocytes when faced with challenging conditions, sooosorption as a response to environmental conditions is relevantacross taxa. Given the established importance of some of thesegroups as models for the study of partial migration (Chapman et al.2011), the potential to investigate the role of reproductive physi-ology in determining individual migratory tendency in othergroups is an exciting avenue for future research.

Acknowledgments

We thank Glenn Holly and Alex Sloane for logistic help duringthe field collection and Charles Fox for providing the Kentuckybugs. Andy Vickers and Salvatore Santandrea provided essentialtechnical help in the realization of the flight mill device. JasonChapman, Ben Chapman and two anonymous referees provideduseful comments on the manuscript. The work was supported by aLeverhulme Grant to T.J.M. and a European Social Funds PhD stu-dentship to A.A.

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