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A Functional System of Adaptive Dispersal by Flight

01 Jan 1966-Annual Review of Entomology (Annual Reviews 4139 El Camino Way, P.O. Box 10139, Palo Alto, CA 94303-0139, USA)-Vol. 11, Iss: 1, pp 233-260

AboutThis article is published in Annual Review of Entomology.The article was published on 1966-01-01 and is currently open access. It has received 70 citation(s) till now. The article focuses on the topic(s): Biological dispersal.

Topics: Biological dispersal (66%)

Summary (2 min read)

Introduction

  • By C. G. JOHNSON Rothamsted Experimental Station, Harpenden, Herts., England Insect dispersal is a confused subject and lacks system.
  • Different people have seen migration and dispersal as distinct, processes, twice reviewed in these volumes.
  • Therefore if a general, valid, and functional system for all of these movements can be made; it may show up effects of incidental and accidental movements in clearer perspective (I suggest that these are small by comparison with those of adaptive move ments) .

PERSPECTIVES OF THE SYSTEM

  • It is often assumed that males and females migrate similarly.
  • Among the latter, some even hibernate where they become adult, dis persing only afterwards [Conophthorus coniperda (71)].
  • Little seems to be known about relative distances travelled by many insects before and after ovipo sition, or between egg laying by the same individuals; but the emigration after pupal emergence (often characterized by a relatively prolonged and undistracted flight), is often the most noticeable with recognized migrants.

PLACE OF ORIGIN

  • There are two fundamentally different types of "populated place " (4) from which dispersal occurs adaptively.
  • Most important is the site where new adults develop.
  • These changes, and those caused by the seasons affect the insects' ontogeny and apparently determine whether or not, or in what proportions, adults will become migrants, and hence the ex tent and amount of dispersal.
  • If Type II movements are migratory in the senses defined earlier (and this is debatable), feeding and oogenesis sites are among these.

EXODUS

  • There are a few observations of the beginnings of "classical" migrations especially of butterflies and dragonflies; rather more exist for migratory in sects in the wider sense, including wind-borne dispersants formerly consid ered to be "passive.".
  • But, of the vast majority of even well known and com mon species, nothing is known about exodus behaviour though it is very im portant for dispersal.
  • The prime function of such flights is departure, sometimes for long distances, as soon as the insects become fully flight-mature.
  • There are more references it seems to the positive act of exodus (few though these are) than to others showing that adults do not leave, and it would be instructive to search out the latter.

TO WEATHER

  • "Flight activity" is a universal term among entomologists.
  • Though these changes are well recognized as long-term trends over several days and even corrected for (169) , their rapidity from hour to hour (when they can simulate the effects of individual responses as far as aerial density change is concerned) is not so well recognized.
  • The duration and progress of this Hight away from the birthplace is adapted to the needs of particular species, varying from a few yards [ter mites, white fly (92)] to thousands of miles (locusts; monarch butterflies) can be resolved into four components: fuel supply ; duration of single flights; and duration of period when such flights are repeatable; and orientation.

ORIENTATION

  • Kennedy et al. (91) inferred that aphids flying near the ground in the "alighting flight" re sponded to both the bright, short wavelengths of the sky and to the dimmer long wavelengths from the green vegetation and were kept in an uneasy bal ance between them, rather than that they became negatively phototactic.
  • The common orientation of butterflies, migrating within the boundary layer, is also apparently established visually at exodus ( 1 10) .
  • Many insects disperse from the birthplace by flying within their bound ary layer and seem to control their track in a more or less linear way ap parently for relatively long distances against or across the wind.

AERIAL TRANSPORT

  • Adaptive displacement per se depends on the following factors; flight speed, duration and frequency of single undistracted flights, the duration of the "migratory" period within which single long flights are made, the need and opportunity to "refuel, " orientation into or out of the "boundary layer, " and the state of the atmosphere.
  • -A complete displacement flight often occurs adaptively both within and above the boundary layer.
  • The ver tical density profile increases in height and decreases in steepness toward mid-day as more i nsects are discharged, and subsides, with the flight rhythm at exodus, to nothing by evening (81, 85) .

THE FIRST HYPOTHESIS

  • The following findings support this hypothesis: Orthoptera migrated when plants dried up and after rain ( 133, 157) .
  • Flight in solitary locusts prob ably was a response to humidity changes (37) .
  • L. cerealium flew en masse when grasses dried up, rather in contrast to normal, prereproductive mass flights (99) .
  • Leafhopper populations moved from cut vegetation (103) .
  • No doubt hunger often causes insects to move but perhaps more to mix than to disperse, for starved insects cannot migrate far (74) .

THE ONTOGENETIC HYPOTHESIS

  • This hypothesis applies, so far, only to females.
  • In large populations of A . monuste, settling thresholds are so high that the insects continue to fly all night (dark ness usually suppresses flight) and into the second day, scarcely stopping more than a few seconds to feed, which prolonged flight makes necessary ; this behaviour is associated with delayed ovarial development ( 1 10) .
  • Johnson, .c. G. A basis for a general system of insect migration and dis persal by flight.
  • Smith sonian Inst. Misc. Collections, 137, 263-86 (1959) Roer, H. Experimentelle Untersuch ungen zum Migrationsverhaltl�n des Kleiner Fuchs (Aglais urticae L.) Beitr.

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
  
         

 

        
          

  


         


Annu. Rev. Entomol. 1966.11:233-260. Downloaded from www.annualreviews.org
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

         
       
         
          
          
 
  
      
    
     
  
       
 

      


        
        


 
    
   

   
    

      
         
       
        
       
            
 

           
   
  
       

  
    
         





   
          




  
       

 
Annu. Rev. Entomol. 1966.11:233-260. Downloaded from www.annualreviews.org
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    
 
     
  
  


       



         
       

         
 
      


    

   

   
         

   
    

       



 
         
     
         
   
        
 

         






           
   
       
    
     

  
     


          
Annu. Rev. Entomol. 1966.11:233-260. Downloaded from www.annualreviews.org
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

          
           
 

          

    
           
 
        
       
     
  
     
         

           

         
         
          
         
     

          
  
  
  
         
          
       
     
         

          
   
    
   
       
          
     


  
          
        
  
Annu. Rev. Entomol. 1966.11:233-260. Downloaded from www.annualreviews.org
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   


      
  
       
  



     

      
  
        
           
      
    
          
         

            
        

 
  
     

 
  

  


     



      
   

      



            
             

        


   


  
    
             
Annu. Rev. Entomol. 1966.11:233-260. Downloaded from www.annualreviews.org
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BookDOI
01 Jan 1978

324 citations


Journal ArticleDOI
Hugh Dingle1
24 Mar 1972-Science
TL;DR: The similarities between birds and insects seem sufficient to indicate, at least provisionally, that the theory developed for insects applies also to birds with appropriate modifications for longer life span and more complex social behavior; comparisons between insects and fish lead to the same conclusion.
Abstract: Physiological and ecological results from a variety of species are consistent with what seem to be valid general statements concerning insect migration These are as follows: (i)During migration locomotory functions are enhanced and vegetative functions such as feeding and reproduction are suppressed (ii) Migration usually occurs prereproductively in the life of the adult insect (the oogenesis-flight syndrome) (iii)Since migrant individuals are usually prereproductive, their reproductive values, and hence colonizing abilities, are at or near maximum (iv) Migrants usually reside in temporary habitats (v)Migrants have a high potential for population increase, r, which is also advantageous for colonizers (vi)Both the physiological and ecological parameters of migration are modifiable by environmental factors (that is, phenotypically modifiable)to suit the prevailing conditions Taken together, these criteria establish a comprehensive theory and adumbrate the basic strategy for migrant insects This basic strategy is modified to suit the ecological requirements of individual species Comparative studies of these modifications are of considerable theoretical and practical interest, the more so since most economically important insects are migrants No satisfactory general statements can as yet be made with respect to the genotype and migration Certainly we expect colonizing populiations to possess genotypes favoring a high r, but genotypic variation in r depends on the heritabilities of life table statistics, and such measurements are yet to be made (10, 53) The fact that flight duration can be increased by appropriate selection in Oncopeltus fasciatus, and the demonstration of additive genetic variance for this trait in Lygaeus kalmii, suggest that heritability studies of migratory behavior would also be worth pursuing Most interesting of course, will be possible genetic correlations between migration and life history parameters Also, migration often transports genotypes across long distances with considerable mixing of populations An understanding of its operation therefore carries with it implications for population genetics, zoogeography, and evolutionary theory Finally, at least parts of the above general theory would seem to be applicable to forms other than insects Bird and insect migrations, for example, are in many respects ecologically and physiologically similar Birds, like insects, emphasize locomotory as opposed to vegetative functions during long-distance flight; the well-known Zugenruhe or migratory restlessness is a case in point Further, many birds migrateat nigt at a time when they would ordinarily roost(vegetative activity) Because their life spans exceed single seasons, bird migrants are not prereproductive in the same sense that insect migrants are, and hence reproductive values do not have the same meaning(but note that some insects are also interreproductive migrants) The situaion is complicated further by the fact that in many birds adult survivorship is virtually independent of age so that colonizing ability tends to be also (10, 54) Nevertheless, birds arrive on their nesting grounds in reproductive condition with the result that migration is a colonizing episode It is also phenotypically modifiable by environmental factors, some of which, for example, photoperiod, influence insects as well (55) The similarities between birds and insects thus seem sufficient to indicate, at least provisionally, that the theory developed for insects applies also to birds with appropriate modifications for longer life span and more complex social behavior; comparisons between insects and fish (56) lead to the same conclusion In birds especially, and also in other forms, various functions accessory to migration such as reproductive endocrinology, energy budgets, and orientation mechanisms have been studied extensively (55, 56) But there is need in vertebrates for more data andtheoy on the ecology and physiology of migratory behavior per se in order tobetter understand its evolution and its role in ecosystem function (5, 57) Migration in any animal cannot be understood until viewed in its entirety as a physiological, behavioral, and ecological syndrome

302 citations


Book ChapterDOI
01 Jan 1969

289 citations


Journal ArticleDOI
TL;DR: It is argued that ACSs are “predictably ephemeral” habitats that present a selective environment that is different from that commonly envisioned for disturbed or early successional habitats, and therefore, effective biological control strategies in ACSs must include a landscape ethic that provides an abundance of permanent habitats that can act as reservoirs for indigenous and introduced natural enemies.
Abstract: Biological control strategies that were developed for orchards and forests have had limited success in controling pests in annual crop systems (ACSs). In this paper I will argue that an accurate characterization of the habitat template of ACSs will be a key feature for developing new strategies of biological control for field crops. I argue that ACSs are “predictably ephemeral” habitats that present a selective environment that is different from that commonly envisioned for disturbed or early successional habitats. By drawing on examples from natural ecosystems that are predictably ephemeral, I characterize the types of life cycles and life-history traits that are common in insects that thrive in these types of environments. “Fugitive” or “colonizing” species that evolve in unpredictably disturbed environments usually allocate resources to numerous dormant or vagile propagules at the expense of parental survival. In contrast, many insects that exploit predictably ephemeral habitats respond to disturbance by dispersing to permanent refugia where they delay reproduction, overwinter, and then recolonize the following year. I refer to this strategy as “cyclic colonization” and document its ubiquity in natural and agroecosystems. Cyclic colonizers typically exhibit between-generation developmental flexibility in life-history traits. In many species, “establishment generations” have small or no wings, are behaviorally sedentary, grow rapidly, reproduce at an early age, and have high fecundities. In contrast, “overwintering generations” are well adapted for dispersal to and from permanent habitats (long wings, behavioral tendency for flight, reproductively immature) and for winter survival. Cyclic colonizers are not, necessarily “r-selected,” but rather have generations that alternate between relatively r- and K-selected life-history traits. Cyclic colonization explicitly relies on spatial heterogeneity, and therefore, effective biological control strategies in ACSs must include a landscape ethic that provides an abundance of permanent habitats that can act as reservoirs for indigenous and introduced enemies. The development of an optimal agricultural landscape for biological control in ACSs will require a metapopulation approach that focuses on annual cycles of colonization between permanent refugia and a patchwork of crop fields. Finally, given the ubiquity of cyclic colonization in ACSs, it seems that effective biological control will depend on an increased information base about the seasonal cycles, dispersal behavior, and overwintering ecology of indigenous and introduced natural enemies.

288 citations


Book ChapterDOI
01 Jan 1978
TL;DR: Water-striders of the genus Gerris Fabr consist of a small group of predatory bugs living on the water surface, and gerrids overwinter on dry land as imagos.
Abstract: Water-striders of the genus Gerris Fabr. consist of a small group of predatory bugs living on the water surface. In temperate climates the habitats often freeze in the winter, and gerrids overwinter on dry land as imagos. The morphology of the species restricts them to habitats protected from wave action. Many of such sites dry up temporarily, but permanent sites also exist.

189 citations


References
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Journal ArticleDOI
01 Mar 1961-Nature

2,196 citations


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Abstract: CONTENTS

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501 citations


Journal ArticleDOI
TL;DR: Analysis of the numbers in flight in the open of five very different species of insect in relation to air temperature finds both the effect of temperature on flight and methods suitable for its evaluation, in terms of this hypothesis.
Abstract: Many attempts have been made to relate the numbers of insects in flight to some function of air temperature both outside and in the laboratory. The subject is complicated in nature because temperature affects both the level of population and the amount of activity of those insects able to fly. Natural populations are usually sampled by traps and current methods of analysis often attempt, first, to distinguish between population changes and behaviour changes and then to relate behaviour, or the amount of activity, to temperature by regression analysis of catches. The method has been applied with outstanding success by Williams (1940, 1961) to large taxonomic groups; its use is based on the hypothesis that activity increases gradually with increase in temperature up to an optimum; above this, further temperature increase causes a fall in activity. Linear regressions are fitted over short temperature ranges and the regression coefficients are positive up to the optimum and negative above it. The whole response curve has recently been demonstrated by Williams & Osman (1960) using trap catches from Egypt where monthly mean temperatures ranged widely enough to show the rise to the optimum, 18-29? C, and the decline above it, 29-34? C. In laboratory cages the number of flights made per minute by individuals of a single species frequently gives a similar response curve, one that rises gradually with temperature to an optimum and then falls gradually to zero, so that some laboratory results appear to be complementary to the regression analysis used by Williams. But flight in cages, being restricted, is not typical of free flight in the open and the number of flights per minute is very much affected by these experimental limitations. Also the increase in numbers flying in the open as temperature increases, shown by trap catches of large taxonomic groups, is caused by the increasing number of species in flight as well as by the number of individuals of each species. Suppose that each individual insect can fly only between two fairly clearly defined temperatures, a lower threshold and an upper threshold, and that all insects of the same species in the same local situation have similar thresholds, i.e. that temperature thresholds are species specific. Then between these two thresholds, the proportion of insects in flight may well be independent of temperature. Hence regression methods may not be appropriate for the analysis of the temperature responses of single insect species. I have therefore analysed the numbers in flight in the open of five very different species of insect in relation to air temperature, to investigate both the effect of temperature on flight and methods suitable for its evaluation, in terms of this hypothesis. However, activity and population changes are chronological processes and trap catches are rarely instantaneous. I have therefore re-examined what a trap catch represents before attempting analysis and, after analysis, the results are considered in the light of laboratory observations.

420 citations