d'H · 2004-11-28 · efficaces (Ehler et Miller 1978; JeMs et Kidd 1996; Elliot et a. 1996; Hodek...
129
Huit especes de coccinelles sont asçociées au puceron Mindarus abietinus Koch en 1996 à Sawyervile, Québec. Deux espèces, Anatis mal) Say et Hannonia axyridis Pallas étaient dominantes et représentaient plus de 96% de tous les individus observés. Les adultes et les larves de l'espèce indigène A. mali apparaissent plus tôt, se déplacent plus rapidement st sont également plus actifs dans la prédation de ce pucerop que ceux d'H axyn'dis. Cette siîuation augmente leur impact sur les populationsdu puceron. La mortalité larvaireatteint 90% pour les deux espèces et la prédation intraguilde est unidirectionnelle en faveur d'A. mali. A l'exception des larves, les stades de ces deux especes ont une distribution différente sur les sapins. L'exclusion manuelle des oeufs de coccinelles a été utilisée pour mesurer l'impact de la prédation exercée par les larves de coccinelles sur M. abietinus. La prédation des larves ne peut prévenir le dommage sur les arbres mais elle réduit le pourcentage de colonies actives et le nombre de pucerons dans les colonies restantes. Cette situation provoque une réduction de la densité des oeufs du puceron et une augmentation de la croissance des pousses annuelles. Finalement, Podabms mgosulus Leconte est signalé pour la première fois comme cantharide prédateur de ce puceron. Ce dernier est un opportuniste qui apparaît tardivement dans le cycle annuel du puceron mais il contribue également à réduire les dmsités de pucerons. Richard Berthiaume
Transcript of d'H · 2004-11-28 · efficaces (Ehler et Miller 1978; JeMs et Kidd 1996; Elliot et a. 1996; Hodek...
Huit especes de coccinelles sont asçociées au puceron Mindarus abietinus
Koch en 1996 à Sawyervile, Québec. Deux espèces, Anatis mal) Say et Hannonia
axyridis Pallas étaient dominantes et représentaient plus de 96% de tous les
individus observés. Les adultes et les larves de l'espèce indigène A. mali
apparaissent plus tôt, se déplacent plus rapidement st sont également plus actifs
dans la prédation de ce pucerop que ceux d'H axyn'dis. Cette siîuation augmente
leur impact sur les populations du puceron. La mortalité larvaire atteint 90% pour les
deux espèces et la prédation intraguilde est unidirectionnelle en faveur d'A. mali. A
l'exception des larves, les stades de ces deux especes ont une distribution différente
sur les sapins. L'exclusion manuelle des oeufs de coccinelles a été utilisée pour
mesurer l'impact de la prédation exercée par les larves de coccinelles sur M.
abietinus. La prédation des larves ne peut prévenir le dommage sur les arbres mais
elle réduit le pourcentage de colonies actives et le nombre de pucerons dans les
colonies restantes. Cette situation provoque une réduction de la densité des oeufs
du puceron et une augmentation de la croissance des pousses annuelles.
Finalement, Podabms mgosulus Leconte est signalé pour la première fois comme
cantharide prédateur de ce puceron. Ce dernier est un opportuniste qui apparaît
tardivement dans le cycle annuel du puceron mais il contribue également à réduire
les dmsités de pucerons.
Richard Berthiaume
Avant-propos
Ce mémoire de maîtrise s'insctiî dans un vaste programme de recherche
financé en grande partie par une subvention de recherche du ministére de
l'environnement et de la faune du Québec visant à mieux comprendre la biologie du
puceron des pousses du sapin dans les plantations d'ahres de Noël au Québec.
L'étude des ennemis naturels attaquant le puceron des pousses du sapin est l'un
des objectifs fondamental de ce programme de recherche. J'ai recueilli les données
sur le terrain concemant les ennemis naturels, effectué l'analyse des données et
écrit les différents chapitres qui constituent ce mémoire.
Je tiens à remercier sincèrement mon directeur de rnémoire M. Conrad
Cloutier pour ses judicieux conseils qui ont permis d'améliorer grandement la qualité
des différents chapitres de ce rnémoire. Je tiens également à exprimer ma profonde
gratitude à mon CO-directeur spirituel M. Christian Hébert du sewice canadien des
forêts pour le support moral ainsi que les précieux conseils qui ont grandement
contribué à améliorer la qualité de ce rnémoire. Je tiens également à le remercier
pour les nombreuses heures qu'il a investi dans la révision des différents articles
constituant ce mémoire ainsi que les nombreuses heures consacrées à discuter
pour entretenir et nourrir la flamme de la passion entomologique.
Je tiens également à remercier Mme Carole Germain, M. Luc St-Antoine et
M. Jean Thibault pour leur support moral de même que pour l'aide technique qu'ils
ont apportke dans la réalisation de ce projet. Je veux également remercier M.
Georges Pelletier pour son aide taxonomique ainsi que M. Jean-Marie Perron pour
m'avoir permis de travailler à la collection du musée de l'université Laval.
Un merci particulier doit également être adressé à M. Daniel Maquis,
producteur, qui m'a permis de réaliser mes travaux à l'intérieur de sa plantation
III
d'arbres de Noël. En tenninant, je voudrais remercier ma famille ainsi que Nathalie
Desrosiers pour leur support.
Table des matières
Résumé ................................................................................................................. I
Avant-propos ......................................................................................................... II
Table des matières ................................................................................................ IV
Liste des figures .................................................................................................... VI
Liste des tableaux .............................................................................................. Vlll
Introduction générale ............................................................................................ 1
A) Problématique du puceron des pousses du sapin ................................ 2
................................... B) Cycle annue! du puceron des pousses du sapin 3
C) Connaissance actuelle des ennemis naturels ....................................... 4
D) Evaluation du potentiel des coccinelles comme prédateurs ................. 6
E) Impact des larves de coccinelles sur le ravageur ................................. 7
F) Podabrus rugosulus une nouvelle espèce de prédateurs ..................... 8
CHAPITRE 1: Exploitation strategies of an indigenous and an exotic coccinellid
predaton of the balsam twig aphid Mindarus abietinus Koch (Homoptera:
Aphididae). in Christmas tree plantations ............................................................. 9
Abstract .................................................................................................... 10
Résumé ..................................................................................................... 11
Introduction ............................................................................................... 12 Material and Methods ................................................................................ 13
Results .................................................................................................. 15
Discussion ................................................................................................... 20 References cited ................................................................................... 30
CHAPITRE 2: CoccineIlid lanml predation on the balsam îwig aphid. Mindarus
abietinus Koch (Homoptera: Aphididae). in a Christmas tree plantations. with
particular emphasis on Anatis mali Say (Coleoptera . Coccinellidae) ................... 61
Abstra ct. ..................................................................................................... 62
Résumé .................................................................................................. 63
Introduction .............................................................................................. 64
Material and Methods ........................................................................... 65
Results ................................................................................................... 67
Discussion ................................................................................................ 69
References cited ...................................................................................... 73
CHAPITRE 3: Podabms rugosulus Leconte (Coleoptera: Cantharidae): an
opportunist predator of the balsam îwig aphid. Mindarus abietinus Koch (Homoptera:
Aphididae). in Québec Christmas tree plantations .............................................. 86
Abstract ..................................................................................................... 87
Résumé .................................................................................................... 88
Introduction ............................................................................................... 89
Material and Methods ................................................................................ 89
Results ...................................................................................................... 91
Discussion .................................................................................................. 92
References cited ....................................................................................... 94
Conclusion générale ............................................................................................... 102
Références bibliographiques ................................................................................ 108
Liste des figures
CHAPITRE 1
Figure 1: Seasonal changes in density of the two dominant coccinellid species and
balsam twig aphid density in a Christmas tree plantation, A) A. malt B) H. axyridiiç;
C) M. abietinus ..................................................................................................... 42
Figure 2: Type of prey attacked by spring adults of two coccinellid species, A) A. mali
and B) H. axyridis ................................................................................................. 44
Figure 3: Seasonal trends in behaviour of adults of A. mali (A) and
H. W d i s (B) ....................................................................................... 46
Figure 4: Seasonal trends in behaviour of larvae of A. mal! (A) and
H. ayid is (B) ....................................................................................... 48
Figure 5: Seasonal trens in adult distribution in balsam fir trees for A. mali (A) and H.
axyridis (B) ......................................................................................................... 50
Figure 6: Seasonal trends in larval distribution in balsam fir trees for A. mali (A) and
H. a~yridis (B) .................................................................................................... 52
Figure 7: Egg masses distribution as a function of height in trees and year of the
shoots for two coccinellid species attacking the balsam twig aphid, A) A. malt B) H.
&dis ............................................................................................... 54
Figure 8: Pupal distribution as a function of height in trees and year of the shoots for
two coccinellid species attacking the balsam twig aphid, A) A. malt B) H.
W d i s .............................................................................................. 56
Figure 9: Cumulative recwitment of eggs, lame. pupae and summer adults for the
two dominant coccinellid species, A) A. maliand B) H. axyridis ........................... 58
Figure 10: Conceptual model of cannibalism and intraguild predation for two
coccinellid species, A. mali and H. axyridis based on obse~ation in Christmas tree
plantations in 1996 Sawye~ille, Québec ............................................................. 60
CHAPITRE 2
Figure 1: Variation with time in percentage of active colonies of the balsam twig
aphid (at least one live aphid per shoot) in balsam fir trees with and without
coccinellid larvae ................................................................................................. 81
Figure 2: Variation with time in dens.ky of the balsam twig aphid in colonies (empty
colonies were excluded) in balsam fir trees with and without coccinellid
larvae ................................................................................................................. 83
Figure 3: Average number of 4'instar or adult viviparae of the balsam twig aphid
eaten by each larval instar of Anatis mali fed ad libitum under laboratory . .
conditions .............................................................................................. 85
CHAPITRE 3
Figure 1: Seasonal trends in captures of P. rugosulus (Nltraplday) in Malaise traps
and M. abietinus alates (Nltraplday) with yellow sticky trap used in two untreated
commercial Christmas tree plantations near Sherbrooke (A and B). Balsam twig
aphid (Nlapex) and P. rugosulus (Nltree) density in the Sawyerville plantation of
.............................................................................. balsam fir (C), Québec in 1996 99
Figure 2: Seasonal trends of Podabrus rugosulus behaviour (A) and distribution on
balsam fir trees (B) in a commercial Christmas tree plantation in Sawyewille.
Québec in 1996 ............................................................................................... 101
Liste des tableaux
CHAPITRE 1
Tableau 1: Coccinellid species abundance and morphs of the balsam twig aphid
attacked in a commercial Christmas tree plantation in 1996 ................................. 38
Tableau 2: Relative importance of predators on A. maliand H. w d i s pupae .... 39
Tableau 3: Percentage mortality of pupae of two coccinellid species as a function of
......................................................... their location on trees (shoot age and thirds) 40
CHAPITRE 2
Tableau 1: Impact of coccine!lid lawal predation on balsam twig aphid egg density,
.................................. tree damage, and tree leader and terminal shoot lengths 79
CHAPITRE 3
Tableau 1: Total capture of M. abietinus and P. rugosulus adults in Malaise traps
used in four commercial Christmas tree plantations near Sherbrooke, Québec, in
....................................................... 1996 and description of surrounding habitats 97
Introduction générale
La lutte biologique englobe l'ensemble des procédés qui tentent de diminuer
de manière significative les densités de population d'un organisme, habituellement
un ravageur, suite à l'action directe de prédateurs. parasites ou pathogènes
manipulés par i'homme (DeBach 1974; Howarth 1991; Cloutier et Cloutier 1992;
Wright et Verkerk 1995). Dans de nombreux systèmes, la lutte biologique est une
altemative viable et efficace à l'utilisation des insecticides de synthèse (Simberloff et
Stiling 1996; Van Driesche et Bellows 1996). Elle permet de diminuer l'utilisation de
ces produits et ainsi limiter leurs effets négatifs sur l'environnement (Cloutier et
Cloutier 1992; Van Driesche et Bellows 1996) et la faune non visée (Reinert 1978;
Cockfield et Potter 1983; Arnold et Potter 1987; Rondeau et DesGranges 1991;
Roger et a. 1994).
Cependant, avant d'envisager l'utilisation de la lutte biologique dans un
système donné, il est essentiel d'identifier les ennemis naturels et de connaître la
biologie et l'écologie des principales espèces attaquant un ravageur particulier
(Hodek 1967; Rice et Wilde 1988). Plusieurs caractéristiques biologiques et
écologiques sont importantes dans l'évaluation du potentiel des ennemis naturels
comme agents de lutte biologique (Gumey et Hussey 1970; Elliott et a. 1996;
Hodek et Honek 1996). Des caractéristiques comme l'efficacité de recherche, la
voracité. la synchronie saisonnière avec la proie, le taux d'accroissement naturel, la
réponse numérique, la capacité de dispetsion, la spécificité vis-à-vis de la proie et
l'adaptabilité climatique sont généralement recherchées chez des ennemis naturels
efficaces (Ehler et Miller 1978; JeMs et Kidd 1996; Elliot et a. 1996; Hodek et
Honek 1996). Cependant, il n'est pas nécessaire de retrouver toutes ces
caractéristiques chez une même espèce d'ennemi naturel pour qu'elle soit efficace
contre un ravageur particulier (Hodek et Honek 1996).
L'évaluation de l'efficacité des ennemis présents naturellement est donc la
première étape dans le développement d'un programme de lutte biologique viable
(Rice et Wilde lo88). II sera par la suite possible, si cela s'avère nécessaire, de
tenter de favoriser les populations d'ennemis naturels pour augmenter leur efficacité
contre l'insecte ravageur (Tamaki et a. 1981; Rice et Wilde 1988; Hodek et Honek
1996). Plusieurs méthodes ont déjà été utilisées pour favoriser les populations
d'ennemis naturels comme par exempk l'aménagement d'abris d'hivemement ou
des sources de nourriture altemative (Ben Saad et Bishop 1976; Mensah et Madden
1994), la modification des pratiques culturales (Andow et Rish 1985; Coderre et a. 1989) ou encore l'augmentation des densités d'ennemis naturels par des lachers
inondatifs (Reyd et Le RÜ 1992; Dreistadt et Flint 1996).
A) Problématique du puceron des pousses du sapin
La culture du sapin baumier (Abies balsamea Mill.) pour la production
d'arbres de Noël est une industrie importante au Canada Au Québec seulement,
plus de 32 millions d'arbres sont cultivés pour la production d'arbres de Noël. Le
puceron des pousses du sapin, Mindarus abietinus Koch., est l'un des principaux
ravageurs de cette culture sous nos latitudes (Deland et &. 1998). Comme son nom
l'indique, ce puceron s'attaque principalement aux conifères du genre Abies, mais il
peut également utiliser d'autres essences conifériennes (Va* 1966; Bradbury et
Osgood 1986; Rather et Mi11s 1989).
Le puceron des pousses du sapin, comme la majorité des pucerons en milieu
forestier, n'est pas un ravageur imporiant des peuplements naturels puisqu'il
n'affecte pas la survie ni la croissance en hauteur et en diamètre des arbres infestés
(Varty 1968; Rose et Lindquist 1994). Cependant, ce puceron a un impact
économique en plantations d'arbres de Noël puisqu'il affecte directement la qualité
esthétique des arbres cultivés (Renault 1983; Bradbuty et Osgood 1986; Rose et
Lindquist 1994; Kleintjes 1997; Deland et a. 1998). Les dommages sont causés par
les colonies qui se développent sur les pousses de l'année courante durant leur
période d'élongation. Ils se manifestent par le recroquevillement des aiguilles et le
rabougrissement de la pousse infestée (Renault 1983; Bradbury et Osgood 1986;
Rather et Mills 1989). Les dommages ainsi créés sont visibles durant quelques
années sur les arbres infestés (Nettleton et Hain 1982) et la croissance élongative
des pousses de I'année courante est limitée lorsque ces dernières sont infestées
par d'importantes populations de pucerons des pousses du sapin (Amman 1963;
Smith et a. 1981; Renault 1983; Rather et Mills 1989).
B) Cycle annuel du puceron des pousses du sapin
Le cycle vital du puceron des pousses du sapin comporte 3 à 4 générations
qui se succèdent de la fin avril jusqu'au début de juillet, soit durant la période
d'élongation des pousses nouvelles du sapin baumier (Varty 1966; Bradbuiy et
Osgood 1986). Au Québec, les oeufs éclosent à la fin avril et au début mai (Deland
et 4. 1998). La première génération de pucerons (fondatrices) s'alimente sur les
aiguilles de I'année précédente puis lorsque les nouvelles pousses commencent à
croître, les fondatrices les colonisent afin de compléter leur développement (Varty
1968; Staiy 1975; Rather et Mills 1989). Lorsque les fondatrices atteignent le stade
adulte, la reproduction parthénogénique commence (Varty 1966, 1968).
La fondatrice et sa progéniture (colonie) s'alimentent alors sur la pousse de
l'année courante et causent les dégâts caractéristiques de ce ravageur (Nettleton et
Hain 1982; Renault 1983; Rather et Mills 1989). La majorité (>go%) des filles de
fondatrices, les vivipares, deviennent à la fin de leur développement des adultes
ailés permettant la dispersion du ravageur (Va@ 1966, 1968; Rather et Mills 1989).
La dispersion peut se faire localement c'est-à-dire d'un arbre à un autre à l'intérieur
d'une même plantation ou à distance, entre deux plantations différentes (Deland et
al. 1998). Les filles de fondatrices dépou~ues d'ailes. les vivipares aptères, se - reproduisent sans se disperser. Leur progéniture sera constituée par la suite
exclusivement des vivipares ailés, petmettant de prolonger la phase de dispersion
du ravageur (Varty 1966,1968; Rather et Mills 1989; Deland et@. 1998).
Après i'envol, les pucerons ailés se déposent sur les arbres pour donner
naissance à la dernière génération, celle des sexués (3e ou 4e selon le cas). Ces
demiers sont aptères et comprennent à parts égales des mâles et femelles (Varty
1966). Après l'accouplement, les femelles sexuées pondent 1 ou 2 oeufs hivernants
(Varty 1968) sur les pousses de sapins de l'année courante (Varty, 1966 Nettleton et
Hain 1982; Rather et Mills 1989; Deland et gi. 1998).
Présentement, la lutte au puceron des pousses du sapin est surtout basée
sur l'utilisation d'insecticides, principalement le diazinon (Kleintjes 1997; Deland et
al. 1998). En plus des effets pernicieux associés à I'utilisaüon de ces produitç sur la - faune non-visée, I'utilisation généralisée du diazinon est soupçonnée d'avoir des
effets négatifs sur certains oiseaux nicheus utilisant ces habitats (Rondeau et
DesGranges 1991). L'utilisation des insecticides élimine aussi les ennemis naturels
(Nettleton et Hain 1982; Kleintjes 1997) qui pourraient contribuer à maintenir les
densités de population du puceron des pousses du sapin à un niveau acceptable
afin de limiter les dégâts sur les arbres.
C) Connaissance actuelle des ennemis naturels
En Amérique du Nord, quelques éiudes ont identifié certains ennemis
naturels associés à ce ravageur (Amman 1963; Varty 1966, 1969; Nettleton et Hain
1982; Kleintjes 1997). Aux Etats-Unis, quelques espèces de coccinelles (Amman
1963; Kleintjes 1997) et deux espèces de Syrphidae (Nettleton et Hain 1982) ont été
retrouvées à l'intérieur de plantations d'arbres de Noël. Au Nouveau Brunswick, les
travaux de Varly (1966 et 1969) en forët naturelle ont aussi permis d'identifier
plusieurs espèces de coccinelles attaquant le puceron des pousses du sapin dont
Mulsantina hudsonica Casey, Anatis mali Say, Chilocorus stigma Say, Coccinella
transversoguffata Fald, Coccinella monticola Muls, Adalia bipunctata L et Adalia
ffigida Schn.. D'autres ennemis naturels appartenant a divers groupes d'arthropodes
ont également été identifiés. Au Québec, aucune étude sur le puceron des pousses
du sapin et ses ennemis naturels n'avait été réalisée avant 1995 en production
intensive d'arbres de Noël.
En 1995, une étude préliminaire des ennemis naturels présents au Québec
réalisée dans des plantations non traitées aux insecticides a permis de constater
une grande diversité d'ennemis naturels attaquant le puceron des pousses du sapin.
Des coccinelles, syrphides, chrysopes et araignées ont alors été identifiés comme
faisant partie de la guilde des prédateurs du puceron des pousses du sapin. Cette
étude préliminaire a pemis de mettre en évidence la présence et l'abondance plus
particulière de la coccinelle Anatis mali Say., mais également d'une coccinelle
récemment introduite, Harmonia axyridis Pallas (Coderre et a. 1995).
Anatis mali est une coccinelle neartique indigène et univoltine qui est
principalement inféodée aux forêts de conifères (Smith 1965a; Gagné et Martin
1968; Watson 1976). C'est également la plus grosse coccinelle du Canada et elle
est largement distribuée en forët boréale (Smith 1965a; Watson 1976). Selon
Kleintjes (1997) cette espèce est particulièrement abondante et consomme
activement ce puceron dans les plantations d'arbres de Noël du Wisconsin. Comme
pour la majorité des coccinelles attaquant des pucerons forestiers (Hams et Bowers
1995), sa biologie est peu connue et son impact sur les densités du puceron des
pousses du sapin n'a jamais été évalué (Kleintjes 1997). Contrairement à A. mali, la
coccinelle H. axyridis est une espèce exotique, originaire de l'Asie du sud (lablokoff-
Khnzorian 1982) et récemment introduite au Québec (Codene et a. 1995). Cette
espèce est considérée comme étant mulrivoltine (lablokoff-Khnzorian 1982) et son
impact sur les densités du puceron est également inconnu.
D) Evaluation du potentiel des coccinelles comme prédateurs
Dans plusieurs agro-écosystemes, les coccinelles peuvent jouer un r6le
régulateur important des populations de pucerons et sont souvent les
entomophages ayant le plus grand impact (Hodek 1967, 1970; Frazer et Gill 1981;
Kring et &.1985; Elliott et Kieckhefer 1990; Campbell et Cone 1994; Hodek et
Honek 1996). Elles possèdent plusieurs caractéristiques recherchées chez les
agents de lutte biologique efficaces (Hodek 1967; Gumey et Hussey 1970). De plus,
leurs populations peuvent parfois être manipulées pour augmenter leur efficacité
prédatrice (Ewert et Chiang 1966; Hodek i967; Hodek et Honek 1996).
Compte tenu des caractéristiques entomophages indéniables des coccinelles
dans de nombreux systèmes et suite aux travaux préliminaires réalisés en 1995,
des études sur cette guilde particulière de prédateurs sont apparues nécessaires.
Le premier objectif de ce mémoire était donc de vérifier le potentiel des différentes
espèces de coccinelles attaquant le puceron des pousses du sapin en étudiant en
conditions naturelles leur synchronie saisonnière, leur phénologie, leur distribution
sur les arbres, leur comportement et leur interaction en fonction du développement
saisonnier de la proie.
Ces observations avaient pour but d'identifier les espèces possédant les
caractéristiques écologiques ou biologiques recherchées pour être intégrées à un
programme de lutte permettant de réduire l'utilisation des insecticides dans ces
milieux. II est essentiel de vérifier le potentiel des ennemis naturels indigènes avant
d'envisager l'introduction de nouvelles espkes d'ennemis naturels comme le
recommandaient Rather et Mills (1 989).
E) Impact des larves de coccinelles sur le ravageur
En plus de vérifier les caractéristiques biologiques et écologiques d'un
prédateur, il est essentiel de mesurer l'impact direct sur les densités du ravageur. La
détermination de l'impact de la prédation exercée par des insectes entomophages
sur les populations de ravageurs représente une difficulté majeure dans l'évaluation
des programmes de lutte biologique (Lapchin et 1987; Luck et a. 1988; Kuno
1991; Bellows et 4. 1992). La technique d'exclusion des ennemis naturels est une
technique appropriée pour estimer leur impact et elle est également la plus
largement utilisée (Luck et 4. 1988; Bellow et &l. 1992; J e ~ k et Kidd 1996). De
plus, en excluant uniquement certains prédateurs attaquant un ravageur particulier
elle permet ainsi d'en mesurer spécifiquement l'impact (Jervis et Kidd 1996). Le
principe de cette approche expérimentale est de comparer la densité du ravageur
entre un milieu ou la prédation n'est pas exclue, et un milieu dépourvu en totalité ou
en partie des prédateurs considérés (Kring et 4. 1985; Luck et &. 1988; Bellow et
al. 1992). -
Plusieurs techniques permettent d'exclure les ennemis naturels (Luck et a. 1988; Bellows et a. 1992; Jemis et Kidd 1996). l'exclusion manuelle étant une
technique directe permettant d'évaluer leur impact (Luck et a. 1988). Elle requiert
une attention continuelle et des visites régulières des plants sur lesquels les
prédateurs sont exclus (Luck et 4. 1988; Hodek et Honek 1996; Jervis et Kidd
1996), mais a l'avantage de mesurer la contribution d'un groupe particulier
d'ennemis naturels (Jervis et Kidd 1996). Elle permet également d'estimer la densité
des prédateurs sur les plants ayant subi une exclusion manuelle (Jervis et Kidd
1996).
Bien que les coccinelles jouent un rôle primordial dans la régulation des
populations de pucerons dans de nombreux systèmes (Hodek 1967,1970; Frazer et
Gill 1981; Kring et a. 1985; Elliott et Kieckhefer 1990; Hodek et Honek 1996), leur
efficacité est largement le résultat de l'action prédatrice des larves (Wright et Laing
1980; Mills 1982). Cependant, dans la majoriîé des études, l'efficacité des adultes
n'a pas été discriminée de celle des larves. De plus, l'efficacité prédatrice des larves
de coccinelles en condition naturelle a r e p peu d'attention dans la documentation
scientifique. Le deuxième objectif de ce mémoire était donc de mesurer I'impact des
larves de coccinelles, principalement celles d'Anatis mali, sur les densités du
puceron des pousses du sapin ainsi que l'effet bénéfique de cette prédation sur la
plante hôte.
F ) Podabrus rugosulus une nouvelle espèce de prédateur
Bien que peu documenté, les Cantharidae sont reconnus comme étant des
prédateurs de pucerons dans de nombreux systèmes (Pimentel et Wheeler 1973;
Vickerman et Sunderland 1975; Sunderland et Vickerman 1980; Mensah et Madden
1994; Stary 1995). Toutefois, aucune étude portant sur le puceron des pousses du
sapin, autant en plantations qu'en forêt naturelle, n'avait rapportée jusqu'à présent,
I'existence de prédateur de cette famille. Le troisième chapitre de ce mémoire
rapporte pour la première fois l'activité prédatrice saisonnière de Podabtus
rugosulus Leconte sur le puceron des pousses du sapin.
CHAPITRE 1
Exploitation strategies of an indigenous and exotic
coccinellid predators of the balsam twig aphid,
Mindarus abietinus Koch. (Homoptera: Aphididae),
in Christmas tree plantations.
Richard ~erthiaume', Conrad Cloutier' and Christian ~éber?
é épar te ment de biologie. Université Laval, Québec
2~ewice canadien des forêts, Région du Québec
Abstract
Eight coccinellid species were found to be asociatad with the balsam twig
aphid in a balsam fir plantation in 1996 at Sawye~ille, Québec, but only five of them
completed a generaîion on this aphid. Two species, A. mali and H. +dis, were
dominant representing more than 96% of al1 adults obse~ed in this Christmas tree
plantation. The indigenous specialist A. mali was cornpared with the recently
introduced generalist H. axyridis to evaluate their potential as predaton of the
balsarn twig aphid. Spring adults of A. mali appeared earlier than those of H. axyndis
and were also more active aphid predators. Oviposition of A. mali began before
aphid population buildup and lawae appeared during Peak population of the aphid.
In contrast, H. axyndis oviposition occuned during peak population of the aphid and
lawae appeared during aphid flight dispersal. Lawae of the indigenous species were
more active and rapid than those of H. axyndis. Mortalii during laival developrnent
reached 90% for both species. Except for lawae, al1 stages of these two coccinellid
species have different distributions on balsam fir trees. During laival development,
intraguild predation was unidirectional in favor of A. mali lawae. Finally, A. mali
increased its population by a factor of thirteen times between spnng and summer
compared to five tirnes for H. axynds.
Résumé
Huit espèces de coccinelles étaient associées avec le puceron des pousses
du sapin dans une plantation de sapin baumier en 1996 à SawyeMlle, Québec.
cependant seulement cinq de ces dernières ont complété une génération sur ce
puceron. Deux espèces, A. mali et H. m d i s , étaient dominantes et représentaient
plus de 96% de tous les adultes observés dans cette plantation d'arbres de Noël.
L'espèce spécialiste indigène A. mali est comparée avec l'espèce généraliste
récemment introduite H. axyridis pour évaluer leur potentiel comme prédateur du
puceron des pousses du sapin. Les adultes pnntanierç d'A. mali sont apparus plus
tôt que ceux d'H. axyndis et ils se sont aussi avérés des prédateurs de puceron plus
actifs. La ponte d'A. mali a débuté avant la reproduction du puceron et les larves
sont appanies durant le pic de population du puceron. Par contre, la ponte d'H.
axyridis est survenue durant le pic de population et les larves sont appanies durant
le vol de dispersion des ailés. Les larves de l'espèce indigène étaient plus actives et
plus rapides que celles d'H. axyndis. La mortalaé durant le développement larvaire a
atteint 90% pour les deux espèces. A l'exception des larves, les stades de ces deux
espèces de coccinelles ont montré une distribution différente sur les sapins. Durant
le développement larvaire, la prédation intraguilde a été unidirectionnelle en faveur
d'A. mali. Finalement, A. mali a augmenté sa population par un facteur de treize fois
entre le printemps et i'été comparativement à cinq fois pour H. axyridis.
Introduction
Numerous predator species are attracted by high aphid populations,
particulariy in monocultures (Kieckhefer and Elliott 1990; Evans 1991). Coccinellidae
is one of the most important arthropod family of aphidophagous predators. and
multispecific associations are common at local aphid outbreaks (Hagen 1962;
Hodek 1970; Kring et gl. 1985; Elliott and Kieckhefer 1990; Evans 1991; Agarwala
and Dixon 1992). In several systems, Coccinellidae play an impottant role in aphid
population regulation and often have the strongest impact among al1 aphidophagous
predaton (Hodek 1967.1970; Kring et a. 1985; Elliott and Kieckhefer 1990; Hodek
and Honek ?996).
The balsam twig aphid. Mindam abietinus Koch., is an important Pest of
balsam fir (Abies balsarnea Mill.) grown as Christmas trees in North America (Varty
1968; Bradbury and Osgood 1986; Rather and Mills 1989; Kleintjes 1997). This
aphid has three or four generations from May to July and it ovenvinters as eggs on
the foliage of the host plant (Amman 1963; Varty 1966; Bradbury and Osgood
1986). Aphids feed on current year shoots causing needle distortion and shoot
stunting. thus reducing the aesthetic value of trees (Amman 1963; Varty 1966;
Nettleton and Hain 1982; Bradbury and Osgood 1986; Rather and Mills 1989;
Kleintjes 1997).
Many coccinellid species have been observed during outbreaks of the balsam
twig aphid either in Christmas tree plar,:Ctions or natural forests (Amman 1963;
Varty 1966, 1969; Rather and Mills 1989; Kleintjes 1997). However, the biology and
ecology of most species are pooriy known. A preliminary inventory carried out in
Christmas tree plantations in Québec in 1995 showed that several species of
Coccinellidae attacked this aphid, Anatis mali Say being the most abundant followed
by Harmonia axynds Pallas which was also commonly encountered.
Although these two species attack al1 instars of the balsam Wig aphid, they
have fundamental differences. Anatis mali is an iridigenous univoltine species which
is closely associated with coniferous forests (Gagné and Martin 1968; Watson 1976)
and. for this reason, this species is considered to be a specialist, with a limited range
of preys and habitats (Smith 1965a; Gagné and Martin 1968; Watson 1976). In
contrast. H. axy& iç a recently introduced multiioltine species originating from
south Asia (Coderre et a. 1995). It feeds on more than one hundred species of
aphids living on various plants and, for this reason, is considered to be a generalist,
with a wide range of preys and habitats (lablokoff-Khnzorian 1982; Hodek and
Honek 1996).
The presence of the recently introduced species, H. axyridis, in the balçam fir
plantation system provides the opportuniiy to compare its exploitation strategies with
those of A. mali. We hypothesized that the indigenous species, A. mali, should have
developed strategies more adapted to exploit the balsarn Wig aphid than H. axyridis
because it evolved with the pest for a much longer period of the. Objectives of this
study were to compare sorne biological characteristics of an indigenous coccinellid
species with those of an exotic species to evaluate their relative potential as
predators of the balsam twig aphid. Comparisons of their phenologies including
host-synchrony, behaviour, distribution in trees and intraguild predation were made
under field conditions.
Material and Methods
Field work was camed out in 1996 in a commercial balsam fir plantation
located near Sawye~ille, Québec (45'201N, 71°341N). CoccineIlid phenologies and
behaviour were studied by examining 30 to 50 randomly selected trees, twice weekly
from May 9 to July 26. Coccinellids were identified to species and stage or instar and
their location on the trees was recorded (upper, middle and lower thirds and shoot
age).
The behaviour of each obsewed coccinellid was classified as local searching
and predation, moving, resting or mating. As they are usually observed in the çame
sequence. local searching and predation were grouped in a single category. Local
searching was defined as the coccinellid searching needles one by one on the çame
shoot. Once found, aphids are usually attacked by the coccinellid. In the case of
predation. the instar of the aphid being consumed by the predator was determined
whenever possible. Moving was defined as rapid walking along the shoot stem axis.
Resting coccinellids were those that remained immobile for a minimum of 10
seconds. Cornplete life cycle of a coccinellid species was recognized when adults
were obsewed in spnng (May and June), lawae andior pupae later in the season
and new adults (usually soft bodied) subsequently in July.
To estimate balsam twig aphid density, four one year old shoots were
collected on each of 10 randomly selected trees twice weekly from Apnl 29 to July
15. Shoots were kept in 100 dram plastic bottles inside a cooler to stop
developrnent. reproduction and predation. They were examined under a
stereomicroscope in the laboratory to count aphids. When buds had opened, the
new growing shoots were also exarnined and aphids were counted on each of them.
Density was expresed as the average number of aphids per apex, an apex being
defined as the shoot of the previous year plus curent year shoots.
To localize oviposition and pupation sites of both coccinellid species and to
detenine mortalii levels of these stages, observations were camed out on 25
randomly selected balsam fir trees before the begining of coccinellid oviposition
(May 22). At 4 days intervals, from May 26 to July 20, egg masses and pupae of
coccinellids were searched, marked and numbered using forestry flags. Coccinellid
species and their location on the tree (upper, middle or lower thirds of trees and
shoot age) were noted for each egg m a s or pupae observed. Moreover, eggs were
counted in each mas.
Previously marked egg masses and pupae were observed at four days
intervals to veriiy hatching or emergence. Three categories of predators attacking
coccinellid pupae and leaving distinct marks on the pupal exuviae were identified.
Goccinellid larvae attacked pupae on their underside while adults attacked them on
the upperside. A pentatomid species, Podisus seneventris Uhl., left a liile hole on
the pupae (direct observation).
The approximate volume of each third of trees was estimated to determine a
theoretical distribution of coccinellid eggs and pupae. Four radius measures (one in
each cardinal direction) were taken at the base of each third of trees (total of 12
measures pertree) and tree height was measured at the end of the growing season.
Using these measures and the cone formula ((radius2*x)'(l/3'~eight)) it was been
possible to estimate the volume of each third of trees.
Results
1. Coccinellid diversity
Eight coccinellid species attacking the balsam twig aphid were found in 1996
(Table l), but only five of these were apparently able to complete one generation
(adult to adult) on this aphid. Anatis mali was by far the dominant species followed
by H. axyndis, these two species together accounting for neariy 97% of al1 observed
individuals coccinellids.
2. Phenology erd host synchrony
The first A. mali adults were observed in an adjacent red pine plantation
(Pinus resinosa Ai.) on one year old shoots of these trees on May 2 and in the
balçam fir plantation one week later. The density increased slowly to reach a
maximum of 2 adults per tree on June 7 (Figure 1). Oviposition began between May
22 and 26 and was completed by June 16, each tree receiving an average of
2 2 4 . 9 B eggs. No A. mali adult was obsewed on trees between June 21 and July
2. The first A. mali lawae appeared on June 4 but none was obsewed on June 7
probably because of poor meteorological conditions. An average maximum density
of 15 larvae per tree was obsewed on June 18. The first pupae appeared on June
21 and new adults emerged from July 5 to 18. An average of 26.6 adults emerged
per tree, representing a densiîy increase factor of 13 w.m respect to the spnng
population.
First adults of H. axyndis were obsewed on May 21 and a maximum density
of 0.5 adult per tree was reached around June 7 (Figure 1). Oviposition began
around May 30 and proceeded to June 24, each tree received an average of
59.9a.0 eggs with a maximum egg density being obsewed on June 12. No adult
was observed on trees between June 21 and July 2. The first H. axyrids lawae were
obsewed on June 14 and a maximum densiîy of 2.9 lawae per tree was reached at
the same date. The four lacval instars were obsewed until mid July. The first pupae
appeared on June 21 and new adults emerged from July 5 to 23. An average of 2.5
adults emerged per tree representing a density increase factor of 5 compared to the
spnng population.
Fundatnces of M abietinus appeared in early May and density remained
relatively constant until May 27 when most of them became adults (Figure 1). Then,
fundatrices moved toward the elongating buds and reproduction began, aphid
density increasing rapidly to reach a maximum of 50 aphids per apex on June 6.
Aphid density within colonies decreased gradually from June 6 to June 24 due to
alates flight dispersal. From June 24 to July 8, near the end of its annual cycle,
aphid density was low.
3. Behavioual observations
From May 9 to 15, adults of A. mali ate only M. abietinus fundatrices and
began to feed on young viviparae forming colonies when they became available on
May 21 (Figure 2). Switching from fundatrices to viviparae occurred 10 days later for
H. axyridis (May 31) (Figure 2). On June 7, only 3% of A. mali adults were eating
fundatrices.
Adults of A. mali were active in early May and mating occurred until the first
week of June (Figure 3). From May 9 to July 18, adults actively searched and
attacked aphids on trees. Adults of H. axyridis appeared later than those of A. mali
and mating was observed from the end of May to the middle of June (Figure 3).
Spring adults of H. axyridis were l e s active in food searching and predation than
adults of A. mali (23.6% vs 65.1%). Summer adults of both species were rnainly
observed resting or mouving toward the top of trees to initiate flight dispersal.
Summer adults were l e s active than spnng adults. but those of A. mali searched
and attacked aphids more frequently than those of M axyridis (41.3OI0 vs 5.7%).
The first A. mali l a ~ a e appeared about 10 days before those of H. axyridis
(Figure 4). From June 4 to 11, little activity was obsewed for A. mali larvae because,
once hatched, ywng larvae remain immobile on their egg m a s (Figure 4). From
June 14 to July 12. A. mali larvae were, on average, more active in searching and
attacking aphids (near 90%) than those of H. axyridis (72.6%). On average, 23.3%
of H. axyridis larvae were observed resting on trees compared to only 6.7% for A.
rnali.
The distributions on trees of both spnng and surnrner adults of A. mali and K
axyridis were different (spnng adults X2261=21 .l6; pcO.001; summer adults X22dl =
58.78; pc0.001). About 50% of al1 spnng adults of A. mali were observed in the
rniddle third of trees, whereas most of H. axyridis aduk were observed in the upper
third (Figure 5). Summer adults of A. mali rnovod to the top of trees to initiate flight
dispersal and their percentage was higher in this portion of the trees. Summer adults
of H. axyridis were mainly found (54.7%) in the middle third of trees, few adults
being obse~ed rnoving to the top of trees to initiate flight dispersal. Futhemore, for
each species the distribution of spring vs surnmer adults was significantly different
(A. maliX22a =l74.18 pe0.001; H. axyridis X2a =24.59 pc0.001).
The lawal distribution in trees of these two species was not significantly
different h22a =0.38; p=0.828) (Figure 6), rnost lawae being found in the lower and
middle thirds where rnost aphid colonies were also obsewed.
4. Distribution of eggs and pupae
Eggs of A. mali were laid in masses of 13.7a.3 eggs, mainly in the lower
third of balsam fir trees (iï.l%), the middle and upper thirds receiving respectively
19.2 and 2.4% of eggs (Figure 7). No egg rnases ware found on current year
shoots and fernales laid their eggs always on the underside of needles or branches
of balsarn fir. H. axyridis egg masses (20.54.2 eggs) were significantly larger than
those of A. mali v482df=-8.114 pc0.001). More than half (56.8%) of H. axyridis eggs
were also laid in the lower third of balsarn fir trees (Figure 7). the rniddle and upper
thirds receiving respectively 24.3 and 18.9% of eggs. Few egg masses were found
on current year shoots. Each tree received an average of 3.0~0.4 egg masses of H.
axyridis compared to 16.4k1.5 egg masses of A. rnali.
Egg m a s distribution was significanly different from a theoretical distribution
based on the volume of each third of trees for A. mali ($261 = 64.633 p<0.001) but
not for H. axyridis (x2m =3.547 p=0.170). Thus, the two species distribute their egg
masses differently in trees k 2 2 ~ =38.689 pc0.001). Dissimilar egg m a s distribution
between these two species exist also when cornpared distribution according to year
of the shoot (X2~a =12.78 p=0.026).
Only 8.73% of A. mali pupae were found in the upper third of trees, the
rernaining being equally distributed between rniddle (44.7%) and lower thirds
(44.4%) (Figure 8). Nearly 50% of A. mali pupae were found on one year old foliage,
16.9% were found on current year shoots. Nearly half of H. axyndis pupae (48.9%)
were found in the rniddle third of the trees, the upper and lower thirds receiving
respectively 16.7 and 34.4% of pupae (Figure 8). Most pupae of H. axyndis (73.3%)
were found on the current year shoots.
Pupal distribution was significantly different from a theoretical distribution
based on the volume of each thid of trees for A. mali h2w =9.663 p=O.008) but not
for H. axyridis pupae h2a 5.853 pd.054). Thus, the two species had different
pupal distribution in trees k2a =8.023 p=0.018). Disçirnilar distribution between
these two species exist also when cornpared pupal distribution according to year of
the shoot h2w =137.12 pe0.001).
5. Mo-liîy and intraguild predation
Curnmulative egg densities were 224.9a.0 and 59237.3 eggs per tree and
average tirnes before hatching were 8 and 6 days for A. mali and H. axynds
respectively (Figure 9). Hatching success was high for both species (99.5% and
9S0/0 for A. mal; and H. axyridk). However, the density decreased strongly between
hatching and pupation for both species. For A. mali, nearly 90% of lawae failed to
reach the pupal çtage cornpared to 93.6% for H. axynds. A. mali adults ernerged 7
days after pupation under field conditions compared to 10 days for H. axyndis. Pupal
mortality was eçtirnated at 11 .O and 32.2% for A. mali and H. axyndis respectively.
For the cornplete generation, A. mali required 10 eggs to produce 1 adult cornpared
to 25 eggs for H. axyndis.
Anatis mali pupae were oiten attacked by adult coccinellids, rnainly by
conspecifics (Table 2). Nyrnphs and adults of Podisus seneventns (Herniptera:
Pentatomidae) were responsible for more than 20% of the total rnortalii of A. mali
pupae. Hannonia axyridis pupae were attacked by adult coccinellids (nearly than
90O/0 of the total mortality) mainly by A. mali. Larvae and adults of P.seneventns also
ate H. axyndis pupae under laboratory condition, but no observation was made
under field conditions. Anatis mali pupae were killed most frequently on peripheral
shoots and predation decreased from the extenor to the interior of the trees (Table
3). Predation on A. malipupae was higher in the upper third of trees.
lntraguild predation was unidirectional in favor of A. mali when 1 invoived
l a ~ a e of the two species of coccinellidae (Figure 10). Anatis mali larvae attacked H.
axyrids larvae of the same or younger instars. However, 4'instar larvae of both
species attacked prepupae and pupae of the other species. Anatis mali larvae and
adults were unidirectional intraguild predators of syrphid larvae (few observations).
Cannibalism was an important mortality factor for A. mali. Larvae attacked larvae of
the same and younger instars. Old larvae (L3 and L4) and adults cannibalized A.
mali prepupae and pupae. Cannibalism was not observed for H. axyndis.
Discussion
Coccinellid communities associated with aphid outbreak are generally
dominated by two to four species representing more than 90% of al1 individuals
(Kring et a. 1985; Agarwala and Dixon 1992; Hodek and Honek 1996). The
coccinellid community was largely dominated by A. mali and H. axyndis which
represented more than 96% of al1 individuals observed during the study. These two
species were abundant in 1996, and thus could be considered as potential biological
control agents against this pest. Other species were not sufficiently abundant in
1996 to have a significant impact on aphid prey. Number of predators in a particular
habitat is an important factor for coccinellid effectivenes in controlling aphids
(Wright and Laing 1980; Mills 1982; Col1 and Ridgway 1995; Hodek and Honek
1996). The indigenous species A. makwas more abundant in 1996 than H. axyridis,
the average adult density per tree being four times higher dunng spnng.
One of the most important factor that determine predator efficacy is
synchrony with prey both in space and t h e (Hagen and van den Bûsh 1968; Hodek
1970; Hodek and Honek 1996). In the study area, ovefintering eggs of M. abietinus
usually hatch in late April and the fi& generation of aphid, the fundatrices, feed on
old needles and do not cause any damage (Varty 1966; Nettleton and Hain 1982;
Bradbury and Osgood 1966; Rather and Mills 1989). Aphid density remains low until
fundatrices become adults and parthenogenetic reproduction begin (Varty 1966,
1968; Bradbury and Osgood 1986).
Natural enemies such as Coccinellidae could have a significant impact on
aphid population if they attack the fundatrices (Kieckhefer and Kantack 1980; Frazer
and Gill1981; Elliott and Kieckhefer 1990). In our study, the two dominant species of
coccinellidae appeared in May but at diierent times. Adults of A. mali appeared in
the first days of May when aphid eggs were hatching while adults of H. axyndis
appeared only on May 21 when fundatrices were mostly in the adult stage and the
reproduction was beginning. Gagné and Martin (1968), also reported early
occurence of A. mali (early May) in red pine (Pinus resinosa Ait.) plantations in
central Ontario. Anatis mali probably killed more fundatrices than H. axyndis
because they were present for a longer period of t h e during fundatrix development
Thus, for the balsam twig aphid, predation on fondatrices could prevent aesthetic
damage that mainly result from feeding by the second generation of this aphid (Varty
1966; Renault 1983; Rather and Mills 1989).
Several factors could explain the earlier occurence of A. mali compared to H.
axyndis in our study. The distance from hibernation sites and the availability of food
are two of the major factors influencing the occurence of Coccinellidae in a particular
habitat (Hodek 1967; Hodek and Honek 1996). According to Hodek and Honek
(1996), many coccinellid species associated to coniferous trees usually retum to
forests for hibemation. The proximity of a 26 years old red pine plantation near the
plantation under study, where A. mali was first observed, might be a suitable habitat
used for hibernation by A. mali. In the paçt, red pine plantations have been reported
to be frequented habitats by A. mali (Gagné and Martin 1968). Hannonia axyndis
usually overwinters in rock cracks and such sites can be far from the breeding
habitat (Obata et d. 1986).
Another factor that could explain the earlier occurence of A. maliis the tirne of
spring ernergence, which is rnainly dependent on species response to ternperature
and photoperiod (Hagen 1962; Hodek 1967; Ongagna and lperti 1994; Hodek and
Honek 1996). Due to different clirnatic adaptations, the indigenous A. malirnay have
emerged earlier than the recently introduced H. axyridis which originales frorn south
Asia. The termination of diapause rnay occur at lower temperatures or shorter
photoperiods for an indigenous species than for an introduced species and thus,
different species rnay not disperse sirnultaneously even if they overwintered at the
sarne site (McMullen 1967; Hodek 1967,1973; Hodek and Honek 1996).
Habitat specificity could also explain the eariier occurence of A. mali.
Stenotopic species like A. mali, which appear to be closely associated to coniferous
fore&, irnrnediately search in a particular h a b i t (Hodek and Honek 1996;
Wissinger 1997). However, eurytopic species, such H. axynds having a large
spectrurn of habitats search food near their overwintering sites, and thus rnay
concentrate in particular habiiats later (Hodek 1967; Hodek and Honek 1996).
Coccinellid oviposition is oiten synchronized with seasonal peaks in aphid
density on particular host plants (Dixon 1970; Honek 1980, Wright and Laing 1980;
Evans and Dixon 1986). Oviposiîion of A. mali began before aphid population
buildup, the maximum being observed during the period of high aphid population
whereas oviposition of H. axyndis began only during the aphid buildup and peaked
when aphid density decreased due to alate flight dispersal. These differences
suggest that A. mali fernales were better synchronized with the balsarn twig aphid
than H. axynds.
Predator-prey synchrony is important to reduce the potential aphid population
buildup, but coccinellids mu9 also be active during the penod preceeding aphid
reproduction (Iperti 1966; Hodek 1967, 1970; Gurney and Hussey 1970; Murdoch
1973; Ehler and Miller 1978; Elliott and Kieckhefer 1990; Elliott et 4. 1996). In our
study, both species of coccinellid were active shortly after their amval on trees, but
A. mali had a longer period for attacking fundatrices because they amved earlier.
Adults of A. mali were also more active and more rapid searchers than aduk of H.
axynds. This should result in a higher impact of A. mali than H axyrids on fundatnx
density. This high searching capacity and mobility of A. mali haç probably evolved
because prey density is usually low in natural coniferow for& (Smith 1965b;
Gagné and Martin 1968; Varty 1969).
Adults A. mali also switched more rapidly to young colonies because they
penetrate the bursting buds while H. axyndis didn't attacked colonies until the shoot
elongation stage. As adult feeding is essential for the production and maturation of
fertile eggs in coccinellid (Ives 1981; Evans and Dixon 1986; Hodek and Honek
1996), the switch of A. mali toward an abundant food resource might have
accelerated its egg maturation. This might explain that A. mali was able to oviposit in
synchrony with colony formation, while H. axyndis oviposition was delayed.
Differential niche selection is an important mechanism that permit
coexistence of species (Rosenzweig 1981; Honek 1985; Coderre and Tourneur
1986; Coderre et a. 1987). Oviposition niche partitioning can be achieved through
factors such as temporal distribution but also through spatial distribution and food
availability (Coderre et a. 1987). For aphidophagous insects, oviposition sites are
important for the survival of young larvae (Hodek 1973; Coderre et gJ. 1987; Kairo
and Murphy 1995; Hodek and Honek 1996). In addition to the differences in timing
of oviposition observed in our study, a difference in oviposition sites on trees was
also observed. Coccinellids usually select oviposition sites in response to the
proximity of food for larvae, optimum microclimatic conditions for development and
protection frorn predators and parasitoids (Evans and Dixon 1986; lperti and Quillici
1986; Hodek and Honek 1996). Although Watson (1976) reported the inverse on
coniferous trees for A. mali, we observed that fernales of this species always laid
their eggs on the underside of needles and srnall branches of balsarn fir. Nurnerous
species including Anatis ocellata L. lay their eggs on the underside of leaves (Kesten
1969; Coderre et 4. 1987). Harmonia axyridis also laid rnost of its eggs on the
underside of needles and srnall branches of balsarn fir, but neady 20% were
observed on the upperside.
The egg distribution of both species varied as a function of height in trees, A.
mali selecting the rniddle and lower thirds while H. axynds showing no height
preference. These distributions rnay reflect two different hunting strategies of the
predator based on the possibility for adults to localize food at distance and the
rnobility of the larvae. lndeed adults of H. axynds can detect prey without direct
contact using olfactory and visual cues (Obata 1986) while A. mali rnay use a
strategy similar to that of A. ocellata which are unable to detect prey before physical
contact (Kesten 1969) like the rnajority of Coccinellidae (Smith 1965b; Hodek 1973;
Carter and Dixon 1982; Obata 1986).
Contrary to H. axyridis, A. mali eggs were rnainly deposited on the lower and
middle thirds of the trees which, given their negatively geotactic and positively
phototactic behaviour (Dixon 1959; Ng 1986; Obata 1986; Hodek 1993) and their
great capacity for movernent (Smith 1965b; Gagne and Martin 1968) would petmit of
larvae to rnove eveiywhere on the trees after hatching. Preferential oviposition of A.
mali in the lower part of trees can also be explained by sorne micro-clirnatic
preferences of this species that evolved in natural coniferous forests or reflect aphid
distribution on trees at the tirne of oviposition.
Balsarn twig aphid colonies develop only on cuvent year shoots and
coccinellid of both species lay their eggs behind these, on old foliage. Coccinellid
larvae are usually positively phototaxic and this leads them to search on branch
apex (Dixon 1959; Ng 1986; Obata 1986; Hodek 1993), which is the region where
balsam twig aphid colonies are found (Varty 1966; Neîtleton and Hain 1982). Egg
deposition on older foliage is thought to be adaptative because it would maximize
larval suwival through the close proximity of food and reduced incidence of
cannibalism (Kairo and Murphy 1995).
Egg masses of A. mali are smaller than H. auyridis but A. mali laid more eggs
masses per tree and thus the number of eggs laid per tree by A. mali was nearly
four times higher than H. axyridis. Abundant oviposition is an important factor
influencing the potential for Coccinellidae to control aphids (Wright and Laing 1980;
Mills 1982; Hodek and Honek 1996).
First larvae of A. mali appeared during peak population of the balsam twig
aphid and the majoriîy hatched during this same period. Coccinellid egg hatching is
often synchronized with seasonal peaks in aphid availabilii on particular host plants
to permit optimal development of larvae on an ephemeral food resource (Honek
1980; Evans and Dixon 1986). Hamonia axynds larvae appeared at the end of
peak aphid population, and the majority of l a ~ a e hatched at the beginning of the
alate flight dispersal. However, larval development period of the smaller H. axyridis
was shorter than for A. mali. Smaller species need less aphids of a given species to
complete larval development than larger ones (Ives 1981; Hodek and Honek 1996).
The potential area that a larva can explore, and thus iis predatory impact is
largely detemined by its moving capaciîy (Dixon 1959, 1970; Carter and Dixon
1984). In Our study, the indigenous A. mali larvae were more active and moved more
rapidly than the introduced H. éxy~fdis. Larvae of both species were more active than
adults in food searching and they have a similar distribution on balsam fir trees, as
they need to find balsam twig aphid where they are.
Despite being relatively unirnpottant egg rnortality was ten tirnes greater for H.
axyndis than for A. mali (5% cornpared to 0.5%). Field observations suggest that
predation on coccinellid eggs was rare or absent in balsarn fir plantation. Egg
rnortality has been reported to be more important in other syçterns, where it reaching
30% (Banks 1956; Dixon 1959; Fox 1975; Mils 1982; Agarwala and Dion 1992)
and resulted rnainly frorn cannibalisrn by eariier hatched larvae. Mortalii within egg
masses depend on hatching synchrony (Banks 1956; Fox 1975). Cannibalisrn
between larvae of sarne egg rnass was observed for A. mali before larval dispersion.
To reduce risks of cannibalisrn, coccinellid fernales should synchronize oviposition
(Aganivala and Dixon 1992).
Mortality during larval developrnent is usually the rnost important cause of
rnortality during immature developrnent (Frazer et gl. 1981) and, in our study, it
reached more than 90% for both coccinellid species, rnortality being slightly higher
for H. axyridis. This rnortalii rnainly resulted frorn cannibalisrn and intraguild
predation. Cannibalisrn has been observed for rnost coccinellid species in natural
populations (Hodek 1967. 1970; Fox 1975; Polis 1981; Polis et gl. 1989; Evans
1991; Spence and Carcarno 1991; Agarwala and Dixon 1992). Stamtion rnay
increase cannibalistic behaviour but it is not essential (Fox 1975; Frazer et 4.1981),
high predator density increases the probability of encounter and aggressive behavior
(Fox 1975; Polis 1981). Srnaller conspecific are more oiten eaten than larger ones
but sorne species attack sarne-sized conspecifics (Polis 1981; Spence and Carcarno
1991; Aganivala and Dixon 1992; Snyder and Hurd 1995). Cannibalisrn is a rnzjor
cause of rnortality in rnany species (Fox 1975; Polis 1981) and also appeared
important for A. mali larvae which attacked any individual of a sarne or srnaller size.
However, although several authors have reported cannibalisrn for H. axyidis
(Dsawa 1989; Hodek and Honek 1996), this behaviour has not been observed in our
study.
intraguild predators of prepupae and pupae. It is the only siage for which H. axynüis
is an intraguild predator of A. mali. This attack was possible because prepupae and
pupae are immobile (Fox 1975; Polis 1981). However, some pupae of A. mali were
able to escape predation by energic up and down movements. Mortalii during pupal
development reached 30% for H. axyndis, mainly resulting from intraguild predation
by A. mali adults. Anatis mali adults emerged eadier than those of H. axynds and
they searched food on the current year shoots where they found pupae of H.
axyndis. Pupal development appears to be shorter for A. mali than H. axyndis and
this increases nsks of predation by A. maliadults on H. axyndis pupae. The duration
of the pupal stage of A. mali was similar to that reported earlier (Gagné and Martin
1968; Smith 1965b). Pupal mortality is higher in the upper part of trees where adults
of A. mai move to initiate flight dispersal. This mcvement increases the probabilii of
encountering pupae. Newly emerged adults were highly vulnerable to predators
during the penod of cuticle hardening. Coccinellid larvae and pupae, mainly A. mali,
were attacked by adults and nymphs of a pentatomid, P.seneventns, which was
responsible for 20% of al1 A. mali pupae eaten.
A. mali apperently increased its population by a factor of thirteen between
spnng and summer compared to fwe for H. axyridis. The number of eggs needed to
produce one adult was lowest for A.. mali (10 eggs) than for H. axyndis (25 eggs). A
higher potential of increase would thus favor A. mali. Adult dispersai after
emergence and the percentage of adult retum for the next season are unknown for
either species and thus, population increase over the breeding season is not a
garranty of succes for the next season.
The fact that H. âxyridis was the second species in importance in this
plantation in 1996 after only three years aiter its first report in Québec (Coderre et a. 1995) indicates that this species has a high potential of establishment in local
agroecosystems. The impact of this new species on indigenous coccinellid
communities cannot be predicted. In many cases, like balsam fir plantations, the
coccinellid community structures, before such introduction, are unknown and the
real impact on indigenous species might remain difficult to establish. This study
perrnitted to evaluate the situation relatively eariy after the introduction and further
research could permit to observe the evolution of this new association. Presently,
the impact of H. axyndis on the dominant inciigenous species, A. mali, does not
seem to be important but if H. axyndis density continue to increase the situation
could change. Moreover, l e s common coccinellid species reported in our study
might have already suffered from this new competitor.
Our results indicate that the indigenous species A. mali is better adapted to
the balsam twig aphid and showed a higher potential for biological control than H.
axyndis in Christmas tree plantations. However, more research is needed to improve
our knowledge on their biology and ecology, particulariy about dispersai after balsam
twig aphid disappearance, and overwintenng sites and mortality. This is essential to
recommend management practices to obtain higher efficacy against the balsam twig
aphid.
References cited
Agatwala, B.K. and A.F.G. Dion. 1992. Laboratoiy siudy of cannibalism and
interspecific predation in ladybirds. Ecol. Entomol. 17: 303-309.
Amman. G.D. 1963. A new distribution record for the balçam twig aphid. J. Econ.
Entomol. 56: 113.
Banks, C.J. 1956. Observations on the behavior and mortaiii in Coccinellidae
before dispersal from the egg shells. Proc. Roy. Entomol. Soc. London. A
31 : 56-60.
Bradbury, R.L. and E.A. Osgood. 1986. Chemical control of balsam twig aphid.
Mindams abietinus Koch (Homoptera: Aphididae). Maine agricultural
experiment station. University of Maine. Technical bulletin 124.12 p.
Carter, M.C. and A.F.G. Dixon. 1982. Habitat quality and the foraging behaviour of
coccinellid lame. J. Anim. Ecol. 51: 865-878.
Carter, M.C. and A.F.G. Dixon. 1984. Foraging behaviour of coccinellid larvae:
duration of intensive search. Entomol. exp. appl. 36: 133-136.
Coderre D. and J.C. Toumeur. 1986. Vertical distribution of aphids and
aphidophagous insects on maize. In: Hodek, 1. (ed.): Ecology of
aphidophaga. Academia. Prague & Dr. W. Junk Dordrecht. pp. 291-296.
Codene, D., Provencher, L. and J.C. Toumeur. 1987. Oviposition and niche
partitioning in aphidophagous insects on maize. Can. Entomol. 119: 195-
203.
Coderre, D., Lucas, E. and 1. Gagne 1995. The occurence of Hannonia axyridis
(Pallas) (Coleoptera: Coccinellidae) in Canada. Can. Entomol. 127: 609-
611.
Coll, M. and R.L. Ridgway. 1995. Functional and nurnencal responses of Orius
insidiosus (Heteroptera: Anthoconda?) to its prey in different vegetal crops.
Ann. Entomol. Soc. Am. 88: 732-738.
Dixon, A.F.G. 1959. An expenmental study of the searching behavior of the
predatory coccinellid beetle Adalia decempunctata (L.). J. Anirn. Ecol. 28:
259-281.
Dixon, A.F.G. 1970. Factors limiting the effectiveness of the coccinellid beetle,
Adalia bipunctata (L.) as a predator of the sycarnore aphid, Drepanosiphum
platanoides (Schr.). Anim. Ecol. 39: 739-751.
Ehler, L.E. and J.C. Miller. 1978. Biological control in temporary agro-ecosysterns.
Entomophaga 23: 207-212.
Elliott, N.G. and R.W. Kieckhefer. 1990. Dynamics of aphidophagous coccinellid
assemblages in small grain fields in eatern south Dakota. Environ. Entomol.
19: 1320-1329.
Elliott, N.C., Kieckhefer, R.W. and W. Kauffman. 1996. Effects of an invading
coccinellid on native coccinellid in an agncultural landçcape. Oecologia 105:
537-544.
Evans. E.W. 1991. lntra versus intenpecific interactions of ladybeetles (Coleoptera:
Coccinellidae) attacking aphids. Oecologia 87: 401-408.
Evans, E.W. and A.F.G. Dixon. 1986. Cues for oviposition by ladybird beetles
(Coccinellidae): response to aphids. J. Anim. Ecol. 55: 1027-1 034.
Fox, L.R. 1975. Cannibalism in natural populations. Ann. Rev. Ecol. Syst. 6: 87-106.
Frazer, B.D. and B. Gill. 1981. Hunger, movernent. and predation of Coccinella
califomica on pea aphids in the laboratory and in the field. Can. Entomol.
1 13: 1025-1 033.
Frazer, B.D., Gilbert, N., Ives, P.M. and D.A. Raworth, 1981. Predator reproduction
and the overall predator-prey relationship. Can. Entomol. 113: 1015-1024.
Gagné, W.C. and J.L. Martin. 1968. The insect ecology of red pine plantations in
central Ontario. Can. Entomol. 100: 835-846.
Gumey, B. and N.W. Hussey 1970. Evaluation of some coccinellid species for the
biological control of aphids in proteded cropping. Ann. Appl. Biol. 65: 451-
458.
Hagen, K.S. 1962. Biology and ecology of predaceous Coccinellidae. Ann. Rev.
Entomol. 7: 289-326.
Hagen, K.S. and R. van den Bosch. 1968. Impact of pathogens, parasites and
predators on aphids. Ann. Rev. Entomol. 13: 325-384.
Hodek, 1. 1967. Bionomicç and ecology of predaceous Coccinellidae. Annu. Rev.
Entomol. 12: 79-1 04.
Hodek. 1. 1970. Coccinellids and the modem pest managent. Bioscience 20: 543-
552.
Hodek, 1. 1973. Biology of Coccinellidae. Academia, Prague & Dr W. Junk The
Haghe. 260 p.
Hodek, 1. 1993. Habitat and food specificity in aphidophagous predators (A review).
Biocontrol Sci. Technol. 3: 91-100.
Hodek, 1. and A. Honek 1996. Ecology of Coccinellidae. Kluwer academic
publishers. Boston. 464 p.
Hoelmer, K.A., Osborne, L.S. and R.K. Yokomi. 1993. Reproduction and feeding
behavior of Delphastus pusillus (Coleoptem: Coccinellidae), a predator of
Bemisia tabaci (Hornoptera: Aleyrodidae). J. Econ. Entomol. 86: 322-329.
Honek, A. 1980. Population density of aphid at the time of settling and ovariole
maturation in Coccinella septempunctata (Coleoptera: Coccinellidae).
Entornophaga 25: 427-430.
Honek, A. 1985. Habitat preferences of aphidophagous coccinellids (Coleoptera).
Entomophaga 30: 253-264.
lablokoff-Khnzorian, S.M. 1982. Les coccinelles (Coléoptères-Coccinellidae) des
régions paléartique et orientale. Editions Boubée. Pans. 568 p.
Iperti, G. 1966. Comportement naturel des coccinelles aphidiphages du sud-est de
la France: leur type de spécificité, leur action prédatrice sur Aphis fabae L.
Entornophaga 2: 203-210.
Iperti, G. and S. Quillici. 1986. Sorne factors influencing the selection of oviposition
site by Pmpylea quatuordecimpunctata. In: Hodek, 1. (ed.): Ecology of
aphidophaga. Academia. Prague 8 Dr. W. Junk. Dordrecht. pp. 137-142.
Ives, P.M. 1981. Feeding and egg production of two species of coccinellids in the
laboratory. Can. Entomol. 113: 999-1005.
Jewis, M. and N. Kidd. 1996. lnsect natural enemies: practical approaches to their
study and evaluation. Chapman & Hall. London. 491 p.
Kairo, M.T.K. and S.T. Murphy. 1995. The l ie histoiy of Rodolia iceryae Janson
(Col., Coccinellidae) and the potential for use in innoculative releases
against lcerya pattecsoni Newstead (Hom., Margarodidae) on coffee. J.
Appl. Entomol. 11 9: 487491.
Kesten. V.U. 1969. Zur morphologie und biologie von Anatis ocellata (L)
(Coleoptera: Coccinellidae). Z. Angew. Entomol. 63: 412-455.
Kieckhefer, R.W. and N.C. Elliolt. 1990. A 13-year suwey of the aphidophagous
coccinellidae in maize fields in eastem south Dakota. Can. Entomol. 122:
579-581.
Kieckhefer, R.W. and B.H. Kantack. 1980. Losses in yield in spring wheat in South
Dakota caused by cereal aphids. J. Econ. Entomol. 31: 455-478.
Kleintjes. P.K. 1997. Midseason insecticide treatment of balsam twig aphids
(Homoptera: Aphididae) and their aphidophagous predators in a Wisconsin
Christmas tree plantation. Environ. Entomol. 26: 1393-1397.
Kring, T.J.. Gilstrap. F.E. and G.J. Michels. 1985. Role of indigenous coccinellids in
regulating greenbugs (Homoptera: Aphididae) on Texas grain sorghum. J.
Econ. Entomol. 78: 269-273.
McMullen, RD. 1967. A field study of diapause in Coccinella novemnotata
(Coleoptera: Coccinellidae). Can. Entomol. 99: 42-49.
Mills, N.J. 1982. Voracity, cannibalism and coccinellid predation. Ann. Appl. Biol.
101: 144-148.
Murdoch, W.W. 1973. The functional response of predators. J. Appl. Ecol. 10: 335-
342.
Nettleton, W.A. and F.P. Hain. 1982. The life history, foliage damage, and control of
the balsam twig aphid, Mindarus abietinus (Homoptera: Aphididae), in fraser
fir christmas tree plantations of western North Carolina. Can. Entomol. 114:
155-1 65.
Ng, S.M. 1986. The geotactic and phototactic responses of four species of
aphidophagous coccinellid larvae. In: Hodek, 1. (ed.): Ecology of
aphidophaga. Academia. Prague 8 Dr. W. Junk. Dordrecht. pp. 57-68.
Obata, S. 1986. Mechanisms of prey finding in the aphidophagous ladybird beetle,
Hamonia axyndis (Coleoptera: Coccinellidae). Entomophaga 31: 303-31 1.
Obata S., Johki, Y. and T. Hidaka. 1986. Location of hibernation sites in the ladybird
beetle, Hamonia axynds. ln: Hodek, 1. (ed.): Ecology of aphidophaga.
Academia. Prague & Dr. W. Junk. Dordrecht. pp. 193-198.
Ongagna, P. and G. Iperti. 1994. Influence de la température et de la photopériode
chez Hamonia axyndis Pall. (Col., Coccinellidae): obtention d'adultes
rapidement féconds ou en dormance. J. Appl. Entomol. 117: 314-317.
Osawa, N. 1989. Sibling and non-sibling cannibalisrn by lame of a lady beetle
Hannonia axyridis Pallas. (Coleoptera: Coccinellidae) in the field. Res.
Pop~l. EcoI. 31: 153-160.
Polis, G.A. 1981. The evolution and dynamics of intraspecific predation. Ann. Rev.
Ecol. Syst. 12: 225-251.
Polis, G.A.. Myers, C.A. and R.D. Holt. 1989. The ecology and evolution of intraguild
predation: potential competiion that eat each other. Ann. Rev. Ecol. Syst.
20: 297-330.
Rather. M. and N.J. Mills. 1989. Possibiiiiies for the biological control of the
Christmas tree pests. the balsarn gall rnidge, Paradiplosis tumifex Gagné
(Diptera: Cecidornyidae) and the balsam twig aphid, Mindarus abietinus
Koch (Hornoptera: Mindaridae), using exotic enernies frorn Europe.
Biocontrol News and Information 10: 1 19-129.
Renault, T. 1983. Puceron des pousses du sapin et cécidornyie du sapin (situation-
1983). Centre de recherches forestières des maritimes. Note technique no
80F. 9 p.
Rosenmeig, M.L. 1981. A theory of habitat selection. Ecology 62: 327-335.
Smith, B.C. 1965a. Differences in Anatis mali Auct. and Coleomegilla maculata lengi
Tirnberlake to changes in the quaiii and quantii of the laml food
(Coleoptera: Coccinellidae). Can. Entornol. 97: 11 59-1 166.
Smith, B.C. 196513. Growth and developrnent of coccinellid lame on dry foods
(Coleoptera: Coccinellidae). Can. Entomol. 97: 760-768.
Spence, J.R. and H.E. Carcarno. 1991. Effects of cannibalism and intraguild
predation on pondskaters (Gemdae). Oikos 62: 333-341.
Snyder, W.E. and LE. Hwd. 1995. Egg-hatch phenology and intraguild predation
between two rnantid species. Oecologia 104: 496-500.
Varty, LW. 1966. The seasonal history and population trends of the balsarn twig
aphid, Mindarus abietinus Koch. in New Brunswick. Forest research
laboratory. Fredericton. 21 p.
Varty, 1.
Varty, 1.
W. 1968. The biology of the balsarn twig aphid, Mindarus abietinus Koch, in
New Brunswick: polyrnorphisrn, rates of developrnent, and seasonal
distribution of populations. Forest research laboratory. Fredericton. 64 p.
W. 1969. Ecology of Mulsantina hudsonica Casey, a ladybeetle in fir-spruce
forest. Forest research laboratory. Fredericton. 28 p.
Watson, W.Y. 1976. A review of the genus Anatis Mulsant (Coleoptera:
Coccinellidae). Can. Entornol. 108: 935-944.
Wissinger, S.A. 1997. Cyclic colonization in predictably epherneral habitats: a
ternplate for biological control in annual crop systems. Biological Control 10:
445.
Wright, E.J. and JE. Laing. 1980. Numerical response of coccinellids to aphids in
corn in southern Ontario. Can. Entornol. 112: 977-988.
Table 1: Coccinellid species abundance and morphs of the balsam twig aphid aitacked in a commercial Christmas tree plantation in 1996.
Species Number Relative obsewed importance (%) -
Anatis mali Say 1425 86,11 Harmonia axyridis Pallas 176 10,69 Coccinella trifasciata L 16 0,97 Coccinella septempunctata L 16 0,97 Mulsantina hudsonica Casey 10 0,60 Chilocorus stigma Say 6 0,36 Adalia bipunctata L 3 0.1 8 Propylea quatuordecimpunctata L 2 0,12
-
Complete Pley generation
Yes F, C, S Yes F, C, S Yes F. C Yes F. C Yes F, C, S No F No C No C
(F) Fondatrix. [C) Colony. [S) ~ G a l ç
Table 2: Relative importance of predators on A. mali and H. axyridis pupae.
Attacked by A. mali H. axyridis
A.mali adulr 20,8 20,7
A-mali 4th instar' 5.6 - Coccinellid lanrae 13,9 3,s
Coccinellid adults 34,7 68,9
P. serieventris adults' 2,8 - P. serieventris lawae' 19,4 -
Unknown 2,8 69
Total 100.0 (MN) 100.0 (2gN)
' Direct observation
Number of pupae obseived
Table 3: Percentage mortality of pupae of two coccinellid species as a function of their location on trees (shoot age and thirds).
Species Shoots Location
96 95 94 93 Upper Middle Lower
A. mali 17,s 8,7 3,6 3,4 13,s 6.7 9,l (112) (321) (138) (58) (58) (297) (309)
H. axyridis 31,8 29,4 50.0 - 40,O 20,s 45,2 (66) (17) (4) (15) (44) (31)
( ) Number of pupae obsewed
Figure 1: Seasonai changes in density of the two dominant coccinellid species and balsam twig aphid density in a Christmas tree plantation, A) P.. rnali; B) H. axyndis;
C) M. abietinus.
120 130 140 150 160 170 180, 190 200 210, 220
May 1 June July
Julian days
Figure 2: Type of prey attacked by spring adults of two coccinellid species, A) A.
mali and B) H. axyndis. The number of adults observed for each date is written
above each bar.
Fundatrix [7 Aphid in colony
2 2 5 27 12 73 72 65 53 53 19 4
Sampling date
Figure 3: Seasonal trends in behaviour of adults of A. rnali (A) and H. axyndis (B).
Number of observations indicated above al1 columns.
Activity
Mating . Local searching and predation
Resting Moving
09 14 15 21 24 28 31 04 07 11 14 18 21 25 28 02 05 09 12 16 19 23 26
May 1 June I July
Sampling date
Figure 4: Seasonal trends in behaviour of larvae of A. mali (A) and H. axyridis (B).
Number of observations indicated above al1 columns.
Activity Local searching and predation
O Resting 17 Moving
04 O7 11 14 18 21 25 28 02 05 09 12 June 1 Juh
Sampling date
Figure 5: Seasonal trends in adult distribution in balsam fir trees for A. mali (A) and
H. axyridis (B). Number of obse~ations indicated above al1 columns.
Thirds . Upper Middle [7 Lower
09 14 15 21 24 28 31 04 07 11 14 18 21 25 28 02 05 09 12 16 19 23 26
May 1 June 1 July
Sarnpling date
Figure 6: Seasonal trends in larval distribution in balsarn fir trees for A. mali (A) and
H. axyridis (B). Nurnber of observations indicated above al1 columns.
Thirds
Upper Middle [7 Lower
June 1 Sarnpling date
05 09 12
July
Figure 7: Egg masses distribution as a function of height in trees and year of the
shoots for two coccinellid species attacking the balsam twig aphid, A) A. mali; B) H.
axyndis.
i A. mali H. axyridis N: 411 N: 74
30 Upper canopy
Others 91 92 93 94 95 96
Year of the shoots
Figure 8: Pupal distribution as a function of height in trees and year of the shoots for
h o coccinellid species attacking the balsam twig aphid, A) A. malt B) H. axyndis.
i A. mali H. axyridis N: 664 N: 90
il -, Lower canopy
20
1 O
O Others 91 92 93 94 95 96
Year of the shoots
Figure 9: Cumulative recruitment of eggs, lawae, pupae and surnrner adults for the
two dominant coccinellid species, A) A. mali and B) H. axyridis.
250
200
150 -A- Adult ernergence
al 100
2 Ci
& 50 P % Ci z O E al 'El
70 .- Ci 0 3 60
J 50 O
40 - Oviposition
30 -A- Adult ernergence
20
10
O 130 135 140 145 150 155 160 165 170 175 180 185 190 l952OO2O52lO
May 1 June 1 July Julian days
Figure 10: Conceptüal model of cannibalism and intraguild predation for two
coccinellid species, A. maliand H. axyridis based on observation in a Christmas tree
plantations in 1996, Sawye~ille Québec.
Anatis mali Harmonia axyridis
C'+aez ~arvae
Prepupae '+, Pupae anci
Adults Adults
CHAPITRE 2
Coccinellid lawal predation on the balsam twig aphid,
Mindarus abietinus Koch (Homoptera: Aphididae),
in a Christmas tree plantation, with pariicular
emphasis on Anatis mali Say (Coleoptera: Coccinellidae).
Richard 6erthiaume1. Christian ~ébert' and Conrad cloufier'
é épar te ment de biologie, Université Laval, Québec
'service canadien des forêts, Région du Québec
Abstract
The impact of natural coccinellid larval predation on balsam twig aphid
populations has been evaluated using hand removal of coccinellid egg masses in a
balsam fir Christmas tree plantationin 1996, in Sawyerville, Québec. Goccinellid
lawal predation did not prevent the formation of damage on trees but it reduced the
percentage of active aphid colonies and aphid density in remaining colonies on
manipulated trees compared to controls. This resuted in a reduction of aphid egg
density and increased growth of current year shoots. Futhermore, coccinellid larval
predation probably decreased the severity of darnage on shoots. Larval predacious
capacity of the most abundant coccinellid species observed in this syçtem, Anatis
mali, was evaluated under laboratory conditions. An average of 2694 4m instar or
adult viviparae of balsam twig aphid were eaten by this species during its larval life.
Résumé
L'impact de la prédation exercée par les larves de coccinelles sur les
populations du puceron des pousses du sapin a été évalué en utilisant l'exclusion
manuelle des oeufs de coccinelles dans une plantation de sapin baumier cultivée
pour la production d'arbres de Noël à Sawyerville, Québec en 1996. La prédation
des larves de coccinelles n'a pas prévenue la formation du dommage sur les arbres
mais elle a réduit le pourcentage de colonies de pucerons actives ainsi que le
nombre de pucerons dans les colonies restantes sur les arbres manipulés
comparativement aux arbres témoins. Cette situation entraîne une réduction de la
densité des oeufs du puceron st une augmentation de la croissance des pousses
annuelles. De plus, la prédation exercée par les larves semble diminuer la sévérité
du dommage sur les pousses annuelles. La capacité prédatrice des larves de
l'espèce de coccinelles la plus abondante observée dans ce système, Anatis mali, a
été évaluée en conditions contrôlées. En moyenne, 269I2 pucerons des pousses
du sapin de 4'"' stade ou adulte de la deuxième génération ont été consommés
par cette espèce durant sa vie larvaire.
Introduction
In several agroecosystems, Coccinellidae play an important rote in regulating
aphid populations, their impact being ofIen the highest of al1 aphidophagous insects
(Hodek 1967,1970; Kring et a. 1985; Elliot and Kieckhefer 1990; Hodek and Honek
1996). Their impact results largely from predation by larval stages (Wright and Laing
1980; Mills 1982). However, in most studies, the predation efficacy of adults vs
larvae has not been discriminated. As the potential of predaton for pest regulation in
natural conditions can only be estimated by direct evaluation (Hodek 1970; Luck et
al. 1988), estimating aphid dens.Q reduction by coccinellid larval predation requires - a comparison of aphid density on plants with or without coccinellid larvae (Hodek
1970; Luck et a. 1988). Such evaluation is important to develop Sound integrated
pest management systems (Rice and Wilde 1988).
The balsam twig aphid, Mindams abietinus Koch., is an important Pest of
balsam fir (Abies balsamea Mill.) grown as Christmas trees in North Amenca (Varty
1968; Bradbury and Osgood 1986). Aphid feeding on current year shoots resuits in
needles distortion and shoots stunting (Varty 1966; Bradbury and Osgood 1986):
Such damage has no commercial impact in natural forests but in Christmas tree
plantations it reduces the aesthetic value of trees and thus has a substantial
economic impact (Rather and Mills 1989; Rose and Lindquist 1994). The balsam
twig aphid has a complex liie cycle requiring three or four generations exiending
from eariy May to late July in Québec (Deland et &. 1998). It overwinters as eggs
laid on the foliage (Varty 1968; Rather and Mills 1989).
Little is known about the biology of natural enemies of the balsam b i g aphid
in North America (Rather and Mills 1989). Coccinellids and syrphid flies (Diptera:
Syrphidae) have been observed preying on this aphid in plantations (Amman 1963;
Neitleton and Hain 1982; Kleintjes 1997) and in natural fore- (Varty 1969).
However, the impact of the coccinellid species obsewed in these studies has not
been estirnated.
In a preliminary inventory of predators, camed out in Christmas tree
plantations in southwestern Québec in 1995, an indigenous coccinellid species,
Anatis mali Say., 'was the rnost abundant predator species suggesting that its
potential to control the balsarn twig aphid rnay be high. This neartic species is the
largest coccinellid in Canada and is widely ditnbuted in boreal forests (Smith
1965a; Watson 1976). However, its biology is poorly known and its potential as
predator to reduce baisam twig aphid density has never been estimated. Other
coccinellid larvae known to be active in this systern in southwestern Québec are
Mulsantina hudsonica Casey, Coccinella septempunctata L., Coccinella trifasciata L.
and Hamonia axyndis Pallas. Objectives of this study were to estirnate the overall
impact of coccinellid larual predation, mainly Anatis mali, on balsam twig aphid
density and on resulting damage and growth of the host plant.
Material and Methods
Field work was camed out in 1996 in a commercial Christmas tree plantation
of balsam fir located near SawyeMlle (45'20'N, 71°34'W) in Québec. Trees were ô-
8 years old and pesticides had never been applied in this plantation. An exclusion
method was used to estirnate the overall impact of coccinellid lawal predation on
balsarn twig aphid density dunng the phase of aphid population growth dunng
reproduction of adult fundatrices. An expenrnental plot of 40 trees was selected (4
rows of 10 trees), in a section where branches of each tree were not touching those
of neighbouring trees so as to limit possible inter-tree dispersal of coccinellid lame.
At least 4 buffer rows were kept around the plot to avoid any edge effect. Twenty
trees were randornly selected in this plot, each tree being allocated to one of the two
treatrnents (coccinellid larval exclusion or control). For the first group of trees,
coccinellid larual predation was excluded by hand rernoval of coccinellid egg masses
at 4 day intervals during the oviposition penod (May 28 to June 13). Exclusion was
succesful as no coccinellid larva was observed on these trees dunng the
experiment. At the beginning of the exclusion (May 28), coccinellid egg density was
detemined by counting eggs on each tree.
1. Impact on aphid density
To estimate the impact of coccinellid larval predation on balsam twig aphid
density. four current year shoots showing signs of aphid activity (needles distortion
andlor honeydew) were collected on each tree at four days intervals from June 13
(beginning of coccinellid egg hatching) to July 17. Shoots were kept individually in
100 dram plastic bottles inside a cooler to stop development, reproduction and
predation on aphids. until their examination under a stereomicroscope to count
aphids in the laboratoty .
To evaluate the possible impact of coccinellid latval predation on balsam twig
aphid egg density, ten current year shoots were collected on each tree on July 28,
when egg laying had been cornpleted. Predation by coccinellid larvae on the
sexuparae generation has the potential to lirnit aphid egg density but since adult
sexuparae are migratory, this needs to be verified. Aphid egg density was estimated
on current year shoots because this has been reported to be the preferred
oviposition site of the balsam twig aphid (Varty 1966; Nettleton and Hain 1982;
Rather and Mills 1989; Deland et 4. 1998). Eggs were counted using a
stereomicroscope in the laboratoty.
2. Impact on tree growth and damage
To evaluate the impact of aphid control by coccinellid lamal predation on tree
growth, two variables of primaty growth were measured at the end of the growing
season (August 22): the length of the tree leader and the length of 20 terminal
shoots randomly selected at mid height in trees.
Damage was estimated on 118 of the tree periphety by counting al1 damaged
and undamaged current year shoots at the end of the aphid's cycle (July 28). A
damaged shoot was defined as a shoot having at least one distorted needle.
3. Predacious capacity of Anatis mali
To determine the predation potenfial of A. mal; on the balsam îwig aphid, the
maximum predacious capacity of its larvae was measured under laboratory
conditions. Twenty five nelvly hatched lame. randomly selected from thirty egg
masses collected in the plantation, were reared individually in 10 cm diameter petri
dishes. They were fed ad libitum with 4'"instar or adult viviparae of the balsam twig
aphid. Lawae were reared at 212Q°C, 60-70% R.H. and 16L:8D. Each day, the
number of aphids eaten and coccinellid larvae instars were determined. The number
of reared coccinellid lawae was reduced to fifteen at the kit instar (4m) because
their voracity was such that providing them for ad libitum feeding became too much
time consuming.
4. Statistical analysis
Mean values were calculated for each tree for aphid density (number per
shoot) and for the length of terminal shoots. Mean values were then cornpared for
trees with and without coccinellid larvae using t-tests. Tree leader length, coccinellid
egg density and the percentage of damage (transformed to arcsindx) were also
submitted to t-tests to compare treatments. Statistical analyses were perfomed
using systatTM (Kirby, 1993).
At the beginning of the experiment (May 28). coccinellid egg density was
similar for the two groups of trees (63.8113.2 vs 70.4i9.7 eggs per tree for the
control and without coccinellid latvae respectively; k0.404; df=18; p=0.691).
After the beginning of coccinellid egg hatching, the percentage of active
colonies (at least one live aphid per damaged shoot) declined progressively for trees
with coccinellid l a ~ a e , while this percentage remained at 100Y0 until June 29 for
trees without coccinellid l a ~ a e (Figure 1). On July 3 and 7. 50% of previously
infested shoots had no aphid for trees with coccinellid lame, compared to only 2.5
and 22.5% for trees without coccinellid larvae.
On June 13, just before the beginning of predation by coccinellid lame,
aphid density in colonies was similar for the two groups of trees (t=-0.57; df=18;
p=0.575) (Figure 2). On June 17, aphid density increased twofold on trees without
coccinellid larvae, but decreased on trees with coccinellid lame. For each sampling
date from June 17 to July 3, aphid density was at least twice higher on trees without
coccinellid larvae compared to trees with coccinellid larvae. and these differences
were significant. On July 7 and 11, near the end of the aphid cycle, differences were
no longer significant between the two groups of trees.
Trees with coccinellid l a ~ a e had a significantly lower mean egg density than
trees without coccinellid larvae, but the percentage of damaged shoots and tree
ieader length were not significantly different (Table 1). However, on trees with
coccinellid larvae, mid-height shoots were significantly longer than on trees without
coccinellid larvae (Table 1).
The number of 4%star or adult viviparae of balsam twig aphid eaten by A.
mal; in laboratory conditions increased with predator l a ~ a l instar (Figure 3). As
expected, maximum consumption was reached at the 4'instar with an average of
190 aphids eaten, representing 71% of the mean total consumption dunng larval life
of A. mal; (269 aphids).
Discussion
Impact assesment of entomophagous insects on pest populations is a major
task in the evaluation of biological control progtams (Lapchin et 4. 1987; Luck et 4. 1988). Whenever possible as here, hand removal of predators is a direct method for
evaluating their impact but this method has received little attention because it
requires continuous attention wich makes the approach tedious (Luck et 4. 1988;
Hodek and Honek 1996; Jervis and Kidd 1996). However, coccinellid egg removal
by hand has a permanent impact on l a ~ a l density after the end of the oviposition
period as practiced in Our study. This method is also advantageous because the
contribution of a particular species or life stages, like coccinellid larvae, to predation
can be assessed directly (Jervis and Kidd 1996). This method also perrnitç to
estirnate predator density on each plant (Jervis and Kidd 1996).
In Our study, there was no difference in coccinellid egg density between the
two groups of trees when the experiment began. Coccinellid females tend to lay their
eggs where they feed and the number of eggs laid is highly dependent upon the
number of aphids eaten (Hagen 1962; Dixon 1973; Ives 1981; lablokoff-Khnzorian
1982; Hodek 1993). It suggests that the number of balsam twig aphids on the two
groups of trees was similar. The percentage of active colonies and the number of
aphids per colony were also sirnilar between the two groups of trees before
coccinellid egg hatching. Thus, the differences between the two groups of trees from
rnid to late June resulted from the absence or presence of coccinellid larval
predation.
Reduction in the percentage of active colonies on trees with coccinellid lame
indicates that these predators can completely destroy balsam twig aphid colonies
once discovered. The efficacy of aphid predators like coccinellid larvae is largely
determined by their voracity (Gumey and Hussey 1970; Mills 1982). In experimental
conditions, larvae of A. mali ate an average of 269 4%star or adult viviparae of
balsam twig aphid which represents seven colonies at the 1996 average density in
field conditions. This is a consenrative estimation bemuse aphid colonies also
contained younger aphid stages. Based on a previous estimation of coccinellid
consumption on the same aphid species (Varty 1969), mean consumption by A. mali
lanrae would be 8.5 times higher than the maximum consumption of Mulsantina
hudsonica Casey larme. The relative duration of each instar and total food
consumption by coccinellid lame can be aifected by several environmental factors,
especially temperature (Gawande 1966; Gumey and Hussey 1970; Obrycki and
Tauber 1981; Hodek and Honek 1996). Total food consumption increases with
temperature and is markedly higher under fluctuating temperatures (Hodek 1970;
Hodek and Honek 1996). Thus, food consurnption by coccinellid lanrae under
experimental conditions is usually underestimating predator potential because they
are usually reared at constant temperatures (Hodek 1970). Thus, the number of
aphid colonies destroyed by coccinellid lawae in our experiment is probably higher
than seven.
It has been shown that coccinellids can prevent aphid population outbreaks in
several systems (Hodek 1967, 1970; Frazer and Gill 1981). In our study, trees
without coccinellid lawae showed an aphid density increase between June 13 and
17. whereas, coccinellid lanral predation prevented this buildup on control trees.
Thus, coccinellid lanrae had an impact on the percentage of active colonies, but also
on aphid density in remaining colonies.
Reduction in the number of aphids per tree due to coccinellid lanral predation
resulted in an increased shoot growth. Several authors reported a reduction of
curent year shoot elongation when balsam twig aphid infestations were severe
(Amman 1963; Smith et ~IJ. 1981; Renault 1983). Presence of coccinellid lanrae on
balsam fir trees did not result in increased height, which is consistent with the fact
that balsam twig aphid does not attack the tree leader (Varty 1966; Nettleton and
Hain 1982; Bradbury and Osgood 1986).
Coccinellid larvae did not reduce the percentage of shoots darnaged by the
balsarn twig aphid because they arrive too late in the phenology of this aphid. Shoot
darnage results frorn feeding by growing colonies produced by fundatrices at the tip
of current year shoots (Va* 1966; Rather and fvlills 1989) and appeared in eariy
June in 1996. At this tirne, coccinellid aduits were ovipositing and eggs had not yet
hatched. Later predation by larvae could not prevent darnage formation on curent
year shoots.
However, coccinellid larvae rnight reduce the severity of darnage on curent
year shoots. Although, this variable was not investigated here, several observations
suggest a potential for reduction in the severity of darnage on new shoots. First,
cornplete de~tniction of a colony by coccinellid larvae should stop the progress of
damage on the shoot and thus reduce the overall severity of darnage. Second, the
reduction of aphid density in colonies should also reduce the severity of darnage on
shoots. Rather and Mills (1989) repotted longer shoots and lower darnage when
balsarn twig aphid density were low. The better growth of new shoots in presence of
coccinellid lawae in this experirnent also indicates lower darnage on these shoots.
In aphid population dynarnics, the impact of natural enernies during the
period following aphid buildup is the rnost irnpottant one for the next generation
(Hodek 1973). During this period, predation by natural enernies should reduce the
density of aphid overwintenng eggs and indirectly the potential nurnber of
fundatrices for the next growing season (Hodek 1973). In our study. aphid predation
by coccinellid larvae during balsarn twig aphid population growth reduced aphid
overwintering egg density by an average of two eggs per curent year shoot. There's
no evidence that coccinellid larvae eat balsarn twig aphid eggs. The reduction
should be attributed to coccinellid larval predation on the preceding stages of the
aphid (apterous fundatrigeniae, alate sexuparae, sexuales) and this should result in
a lower initial fundatrix density for the following spnng.
Manipulating populations of existing natural enemies to improve their
effectiveness against insect pests is an alternative for biological control (Tamaki et
al. 1981; Rice and Wilde 1988). Several methods have been used to manipulate - coccinellids, such as providing shelter for hibernation or altemate food sources
(Hodek and Honek 1996), modification of cultural pratices (Andow and Risch 1985)
and augmentation of population density (Dreistadt and Flint 1996).
Several possibiliiies can be investigated to improve efficacy of coccinellid
lawae to prevent balsam twig aphid damage. One of them is the utilization of
altemative food. A wide range of natural enemies suffer from the lack of pollen or
nectar in pure monocultures (Hodek and Honek 1996). Alternative food is essential
for coccinellids when preferred prey is absent (Hodek and Honek 1996). Alternative
artificial food has been used to atiract coccinellids to the required h a b i i especially
when the pest begin to occur (Ewert and Chiang 1966; Schiefelbein and Chiang
1966; Ben Saad and Bishop 1976; Mensah and Madden 1994). Futhermore,
alternative food may also result in faster ovanan maturation and, thus earlier
oviposition by females. Lawae would hatch earlier, could have a higher impact, and
be more efficient to prevent damage, because they would be bener synchronized
with the formation of balsam twig aphid colonies. Anatis mali might respond
positively to dry altemative food in the field (Smith 1965b).
Demonstrating the impact of coccinellid lawae is an important step to
introduce biological control in Christmas tree plantations. However, more research is
needed to improve our knowledge on their biology and ecology to define specific
management practices aiming to increase their impact against the balsam twig
aphid.
Reierences cited
Amman, G.D. 1963. A new distribution record for the balsam twig aphid. J. Econ.
Entomol. 56: 113.
Andow, D.A. and S.J. Risch. 1985. Predation in diversified agroecosystems: relation
between a coccinellid predator Coleomegilla maculata and its food. J. Appl.
Eco~. 22: 357-372.
Ben Saad, A.A. and G.W. Bishop. 1976. Attraction of insects to potato plants
through use of ariificial honeydews and aphid juice. Entomophaga 21: 49-
57.
Bradbuiy, R.L. and E.A. Osgood. 1986. Chemical control of balsam twig aphid,
Mindarus abietinus Koch (Homoptera: Aphididae). Maine agncultural
expenment station. University of Maine. Technical bulletin 124.12 p.
Deland, J.P., Berthiaume, R., Hébert, C. and C. Cloutier. 1998. Programme
altematif de protection du sapin de Noël contre le puceron des pousses
dans le contexte d'une saine geçtion des ressources environnementales.
Rapport final. Projet de recherche et technologie en environnemEntomo1.
Ministère de l'environnement et de la faune. Québec. 105 p.
Dixon, A.F.G. 1973. Biology of aphids. Edward Arnold (Publishers) Limiîed. London.
58 p.
Dreistadt, S.H. and M.L. Flint. 1996. Melon aphid (Homoptera: Aphididae) control by
inundative convergent lady beetle (Coleoptera: Coccinellidae) release on
Chrysanthemum. Environ. Entomol. 25: 688-697.
Elliot, N.C. and R.W. Kieckhefer. 1990. Dynamics of aphidophagous coccinellid
assemblages in small grain fields in eastem South Dakota. Environ.
Entomol. 19: 1320-1329.
Ewert, B.M. and H.C. Chiang. 1966. Dispersal of three species of coccinellids in com
fields. Can. Entomol. 98: 999-1003.
Frazer, B.D. and B. Gill. 1981. Hunger. movement, and predation of Coccinella
califomica on pea aphids in the laboratory and in the field. Can. Entomol.
113: 1025-1033.
Gawande, R.B. 1966. Effect of constant and alteming temperatures on feeding and
development of Chilomenes sexmaculata Fb. In Hodek, 1. (ed): Ecology of
aphidophagous insects. Academia. Prague & Dr W. Junk. The Hague. pp.
63-67.
Gumey, B. and N.W. Hussey. 1970. Evaluation of some coccinellid spicies for the
biological control of aphids in protected cropping. Ann. Appl. Biol. 65: 451-
458.
Hagen, K.S. 1962. Biology and ecology of predaceous Coccinellidae. Ann. Rev.
Entornol. 7: 289-326.
Hodek, 1. 1967. Bionomics and ecology of predaceous Coccinellidae. Ann. Rev.
Entornol. 12:79-104.
Hodek, 1. 1970. Coccinellidae and the modem peçt management. Bioscience 20:
543-552.
Hodek, 1. 1973. Biology of Coccinellidae. Acadernia. Prague & Dr W. Junk. The
Haghe. 260 p.
Hodek, 1. 1993. Habitat and food specificity in aphidophagous predators (a review).
Biocontrol Sci. Technol. 3: 91-100.
Hodek, 1. and A. Honek 1996. Ecology of Coccinellidae. Kluwer acadernic
publishers. Boston. 464 p.
lablokoff-Khnzorian, S.M. 1982. Les coccinelles (Coléoptères-Coccinellidae) des
régions paléartique et orientale. Editions Boubée. Pans. 568 p.
Ives, P.M. 1981. Feeding and egg production of two species of coccinellids in the
laboratory. Can. Entornol. 113: 999-1 005.
Jemis, M. and N. Kidd. 1996. Insect natural enernies: practical approaches to their
study and evaluation. Chaprnan & Hall. London. 491 p.
Kirby. K.N. 1993. Advanced data analyçis with SYSTAT. Van Nostrand Reinhold CO.
New York. 475 p.
Kleintjes, P.K. 1997. Midseason insecticide treatrnent of balsarn twig aphids
(Hornoptera: Aphididae) and their aphidophagous predators in a Wisconsin
Christmas tree plantation. Environ. Entornol. 26: 1393-1397.
Kring. T.J., Gilstrap. F.E. and G.J. Michels. 1985. Role of indigenous coccinellids in
regulating greenbugs (Hornoptera: Aphididae) on Texas grain sorghurn. J.
Econ. Entomol. 78: 269-273.
Lapchin, L., Ferran, A., Iperti, G., Rabasse, J.M. and J.P. Lyon. 1987. Coccinellids
(Coleoptera: Coccinellidae) and syrphids (Diptera: Syrphidae) as predators
of aphids in cereal crops: a comparison of sampling rnethods. Can.
Entomol. 11 9: 81 5-822.
Luck, R.F., Shepard, B.M. and P.E. Kenmore. 1988. Experirnental rnethods for
evaluating arthropod natural enernies. Ann. Rev. Entornol. 33: 361-391.
Mensah. R.K. and J.L. Madden. 1994. Conservation of iwo predator species for
biological control of Chrysophtharfa bimaculata (Coleoptera: Chrysomelidae)
in Tasrnanian forests. Entomophaga 39: 71-83.
Mills, N.J. 1982. Voracity, cannibalism and coccinellid predation. Ann. Appl. Biol.
1 01: 144-148.
Nettleton, W.A. and F.P. Hain. 1982. The life history, foliage damage, and control of
the balsam twig aphid, Mifidarus abietinus (Homoptera: Aphididae), in fraser
fir chnstmas tree plantations of western North Carolina. Can. Entomol. 114:
155-1 65.
Obrycki, J.J. and M.J. Tauber. 1981. Phenology of three coccinellid species: thermal
requirernents for development. Ann. Entomol. Soc. Am. 74: 31-36.
Rather, M. and N.J. Mills. 1989. Possibilities for the biological control of Christmas
tree pests, the balsarn gall midge Paradiplosis tumifex Gagne (Diptera:
Cecidomyiidae) and the balsarn twig aphid, Mindarus abietinus Koch
(Homoptera: Mindandae), using exotic enernies frorn Europe. Biocontrol
News and information 10: 11 9-129.
Renault, T. 1983. Puceron des pousses du sapin et cecidomyie du sapin (situation-
1983). Centre de recherches forestières des maritimes. Note technique No
80F. 9 p.
Rice, M.E. and G.E. Wilde. 1988. Experimental evaluation of predators and
parasitoids in suppressing greenbugs (Homoptera: Aphididae) in sorghum
and wheat. Environ. Entomol. 17: 836-841.
Rose A.H. and O.H. Lindquist. 1994. Insectes des épinettes, du sapin et de la
pruche de I'est du Canada. Reçççources naturelles Canada. Ottawa. 159 p.
Schiefelbein, J.W. and H.C. Chiang. 1966. Effects of spray of sucrose solution in a
corn field on the populations of predatory insects and their prey.
Entomophaga 11 : 333-339.
Smith, B.C. 1965a. Differences in Anatis mal; Auct. and Coleornegilla rnaculata lengi
Timberlake to changes in the q u a l i and quantii of the larval food
(Coleoptera: Coccinellidae). Can. Entomol. 97: 11 59-1 166.
Smith, B.C. 1965b. Growth and development of coccinellid larvae on dry foods
(Coleoptera: Coccinellidae). Can. Entomol. 97: 760-768.
Smith, C.C., Newell, W.R. and T.R. Renault. 1981. Common insectç and diseases
of balsam fir Christmas trees. Canadian Foreçtry Service. Technical Note.
No 1328.63 p.
Tamaki. G.. Annis, B., and M. Weiss. 1981. Response of natural enemies to the
green peach aphid in diierent plant cultures. Environ. Entomol. 10: 375-
378.
Varty. I.W. 1966. The seasonal history and population trends of the balsam twig
aphid, Mindarus abietinus Koch, in New Brunswick Forest research
laboratory. Fredericton. 21 p.
Varty, I.W. 1968. The biology of the balsarn twig aphid, Mindarus abietinus Koch, in
New Brunswick: polymorphism, rates of development, and seasonal
distribution of populations. Forest research laboratory. Fredericton. 64 p.
Varty, I.W. 1969. Ecology of Mulsantina hudsonica Casey, a ladybeetle in fir-spruce
forest. Forest research laboratory. Fredericton. 28 p.
Watson, W.Y. 1976. A review of the genus Anatis Muisant (Coleoptera :
Coccinellidae). Can. Entomol. 108: 935-944.
Wright, E.J. and J.E. Laing. 1980. Numerical response of coccinellids to aphids in
corn in southem Ontario. Can. Entornol. 112: 977-988.
Table 1: Impact of coccinellid lawal predation on balsam twig aphid density, tree damage, and tree leader and terminal shoot lengths.
With coccinellid larvae Without coccinellid larvae (Mean t se) (Mean t se)
Aphids egg densiîy (Numberl shoot) 5.0 t 0,s 7,3 + 0,4 0,001
Damage (%) 53.5 t 9.4 50,s t 8.0 0,770
Tree leader length (mm) 506 f t 27,4 474,l t 31,s 0,451
Terminal shoot length (mm) 152.9 t 2,s 128,5 t 3,O 0,001
Figure 1: Variation with time in percentage of active colonies of the balsam twig
aphid (a! least one live aphid per shoot) in balsam fir trees with and without
coccinellid lawae.
Figure 2: Variation with time in dens'Q of the balsam twig aphid in active colonies
(empty colonies were excluded) in balsam fir trees 4th and without coccinellid
latvae. For each date, different lettes indicate significüiit differences.
Figure 3: Average number of 4%star or adult viviparae of the balsam b i g aphid
eaten by each larval instar of Anatis malifed adlibitum under laboratory conditions.
(as r )O uap?a sp! y d y -
CHAPITRE 3
Podabrus rugosulus Leconte (Coleoptera: Cantharidae):
an opportunist predator of the balsam twig aphid,
Mindarus abietinus Koch (Homoptera: Aphididae),
in Québec Christmas tree plantations.
Richard 6erthiaume1, Christian ~ é b e r t ~ and Conrad ~loutier'
op épar te ment de biologie, Université Laval, Québec
'service canadien des forëts, Région du Québec
Absiract
This is the first report of a canthand predator in the balsarn îwig aphid system,
either in Christmas tree plantations or in natural forests. Podabms mgosulus
Leconte appeared late in the annual life cycle of the balsam twig aphid and could
not prevent darnage formation on trees but they contnbuted to reducing aphid
density. Only adults of this species are predators on the balsam b i g aphid and the
majority of individuals (>85%) were observed preying on the aphid. Adult amval of P.
mgosulus appeared to follow the flight dispersal of balsam twig aphid alates.
Evidence suggest that Podabms mgosulus is an opportunist generalist predator
taking advantage of the balsam twig aphid availabilii at a specific tirne in its annual
life cycle.
Résumé
C'est la première mention d'un cantharide prédateur dans le système du
puceron des pousses du sapin, aussi bien en plantation d'arbres de Noël qu'en forêt
naturelle. Podabrus rugosulus Leconte apparaît trop tardivement dans le cycle
annuel du puceron des pousses du sapin pour prévenir la formation du dommage
sur les arbres. Cependant, il contribue à réduire les densités de pucerons. Seuls les
adultes de cette espèce sont des prédateurs du puceron des pousses du sapin et la
majorité d'entre eux (>85%) ont été O ~ S ~ N ~ S consommant ce puceron. L'arrivée
des adultes de P. nigosulus semble suivre le vol des ailés du puceron des pousses
du sapin. Podabrus r go su lus apparaît comme un prédateur opportuniste
généraliste qui prend avantage de la disponibilité du puceron des pousses du sapin
à un moment spécfique dans son cycle annuel.
Introduction
Many species of Coccinellidae (Coleoptera), Syrphidae (Diptera) and
Chrysopidae (Neuroptera) are known as important predators of aphids (Hagen and
van den Bosch 1968; D ion 1973; Sunderland and Vickerman 1980). However,
species from other arthropod taxa can also contribute to control aphid populations
(Pimente1 and Wheeler 1973; Dunning et & 1975; Edwards et a. 1979; Sunderland
and Vickeman 1980). One such species, Podabm mgosulus Leconte (Coleoptera:
Cantharidae) was observed aitacking the balsam twig aphid, Mindams abietinus
Koch. This aphid is an important pest of balsam fir (Abies balsamea Mill.) grown as
Christmas trees in northeastem America (Varty 1968; Nettleton and Hain 1982;
Bradbury and Osgood 1986; Rather and Mills 1989). This aphid has three or four
generations from May to July, and overwinters as eggs on the foliage of the host
trees. Aphids feed on current year shoots causing needles distortion and shoots
stunting thus reducing the aesthetic value of trees (Amman 1963; Varty 1966;
Nettleton and Hain 1982; Bradbury and Osgood 1986; Rather and Mills 1989).
The biology and ecology of this cantharid beetle are unknown and its
predacious role on balsam twig aphid has never been reported. In this paper, we
describe its seasonal activity on balsam fir grown as Christmas trees near
Sherbrooke, Québec, in 1996, during an infestation of M. abietinus.
Material and Methods
Field work was canied out in 1996 in a commercial Christmas tree plantation
of balsarn fir (Abies balsamea Mill.) located in Sawyerville (4S020'~, 71°34'W) in
Québec. Trees were 6-8 years old and pesticides had never been applied. Twice
weekly from May 9 to July 26 inclusively. 30 to 50 randomly selected trees were
visually examined to i m i e (upper, middle or lower third of the tree crown) and
identify Coleoptera predators.
The activity of each predator was recorded as: local searching and predation,
mating, moving and resting. As they are usually observed in the same sequence,
local searching and predation were grouped in a single categoty. Local searching
was defined as the predator searching needles one by one on the same shoot.
Once found, aphids are usually attacked by the predator. In the case of predation,
the instar of the aphid being consumed by the predator was detennined whenever
possible. Moving was defined as rapid walking along the shoot stem ais. Reçting
predaton were those that remained immobile for a minimum of 10 seconds.
To study the seasonal flight activity predators in the plantation and flight
dispersal of the balsam twig aphid, a Malaise trap was operated from May 8 to
September 30. Malaise traps were also operated in three other balsam fir
plantations (one per plantation) during the same penod, including one (East-Clifton)
without insecticide application, and two (Lennoxville and Cookshire) that were
treated with Diazinon to control balsam twig aphid populations. Malaise traps were
checked twice weekly from May to July, and evety other weekly in August and
September. Each sample was examined under a stereomicroscope in the laboratoiy
to identify and count P. gos su lus adults and M. abietinus alates. Flight dispersal of
the balsam twig aphid was also monitored in the Sawye~ille and East-Clifton
plantations using 326 cm2 yellow sticky traps (Seabright Laboratones, Emeryville,
CA). In these plantations, five traps were installed, one on each of five randomly
selected trees. seperated by a minimum of 20 metres. Traps were placed around
the tree leader, and were renewed twice weekly from June 1 to July 13. Collected
traps were examined under a stereomicroscope in the laboratory to count M.
abietinus alates.
Balsam twig aphid density on trees was estimated twice weekly in the
Sawyerville plantation from April29 to July 15 by collecting four apex per tree on 10
randomly selected trees. An apex was defined as the shoot of the previous year plus
curent year buds or shoots. Apices were kept in 100 dram plastic bottles inside a
cooler to stop development, reproduction and predation on aphids. They were
examined under a stereomicroscope in the laboratory to count aphids.
Resulk
Mindams abietinus fundatrices appeared at the beginning of May, the density
per apex remain;.~g low until the last week of May when they became adults and
parthenogenetic reproduction began (Figure 1C). Aphid densiQ then increased
rapidly to reach a maximum of 50 aphids per apex on June 6. Aiter this peak,
density decreased gradually with flight dispersal of mature alate viviparae.
Podabms rugosufus adults were first obsewed on balsam fir trees on June
11. Their density increased to reach a maximum of 3 adults per tree on June 18
(Figure IC), an6 then decreased gradually, the las3 adult being observed on July 12.
Immatures were not obsewed on balsam fir trees and only one mating was
obse~ed on June 21 (Figure 2A). From June 11 to July 12, rnost P. rugosulus
o b ~ e ~ e d (86.5%) were actively searching and preying M. abietinus on trees.
Predation on balsam twig aphid was mostly obsewed on the alate morph.
Podabrus rugosulus were mainly obsewed in the middle third of trees
(51.9%), the upper and lower thirds receiving respectively 26.9 and 21.7% of al1
individuals obsewed (Figure 28). Their distribution ~ r i e d liile during the season.
In Malaise tmps, P. rugosulus was caught only in the two untreated
plantations and total numbers of balsam twig aphid alates caught were at least 10
times higher in these plantations (Table 1). The first captures occurred after the
beginning of alate dispersal on June 13 and 17 respectively for these two plantations
(Figure 1A and B). The lower number of P. mgosulus caught on June 25 resulted
from poor meteorological conditions (min) in the previous days. The number of
individuals caught was higher for the Sawyewille plantation (Table 1) and the period
of activity was earlier, like the balsam twig aphid alate dispersal, compared to the
East-Clifton plantation (Figure 1).
Discussion
Although Cantharidae are hown as aphid predators (Pimentel and Wheeler
1973; Vickennan and Sunderland 1975; Mensah and Madden 1994; Stary 1995),
little is known about their biology and their influence on prey populations. This is the
first report of a canthand predator, in the balsam twig aphid çyçtem, either in
Christmas tree plantations or natural forests. This was not an isolated case since
more than 250 adults of this species were obse~ed, most of them searching or
feeding on the balsam twig aphid. This canthand species has also been obsewed in
other commercial plantations in southem Québec.
The f i n t P. gos su lus appeared late in the annual life cycle of the balsam twig
aphid and thus, cannot prevent damage fonation on trees, which results from
feeding by the second generation of the aphid (Varty 1966; Nettleton and Hain 1982;
Rather and Mills 1989). However, they contribute to reduce aphid density because.
according to Hodek (1973), predation is mainly efficient after aphid buildup, which is
one of the most important penod in aphid population dynamics.
This canthand predator was observed when balsam twig aphid density
decreased on trees during the flight dispetsal of alates. Immature alate dispersal
pnor to flight and alate dispersal might act as a signal retaining searching adults of
this predator in Christmas tree plantations. Absence of P. mgosulus in plantations
where insecticides were applied to control balsam twig aphid support the importance
of aphid populations on trees for attraction and retention of this canthand predator.
During this penod of the annual liie cycle of the balsam twig aphid, mature and
immature alates may be amilable to P. gos su lus as they leave pseudogalls foned
by colonies before taking flight (Variy 1966). Predation on balsam twig aphid was
mostly observed on the adult alate morph outside colonies.
Despite the fact that the aphid alate population at East-Clifion was at least
three times higher than the Sawye~lle population, numencal response of P.
gos su lus was l e s important. This indicates that surrounding habitats around
Christmas tree plantations would be important in the numencal response of this
canthand predator. In fact. P. rugosulus appears as a genoralist opportunisî predator
taking advantage of the balsam twig aphid availabiiii at a specific time in its annual
life cycle.
Despite their late arriva1 into the plantation. adults of P. rugosulus were active
predators, more than 85% being observed while preying on the balsam twig aphid.
This may contribute to decrease the balsam twig aphid density.
Adult P. rugosulus were mainly observed in the middle third of balsam fir
trees. which probably reflects the greater density of the aphid in this portion of trees.
No immatures of this species were found on trees, which is consistent with the fact
that cantharid larvae are mostly predators of Dipterous larvae and other son bodied
insects living in the soi1 (Amett 1963; White 1983).
This study is a first step toward understanding the ecological role of cantharid
beetles as aphid predators. More research is needed to improve our knowledge on
P. mgosulus as a predator of the balsam lwig aphid on Christmas trees.
References cited
Amman, G.D. 1963. A new distribution record for the balsam twig aphid. J. Econ.
Entomol. 56: 113.
Ameît, R.H. 1963. The beetles of the United States (a manual for identification). The
catholic univers'%y of America Press. Washington. 11 12 p.
Bradbury, R.L. and E.A. Osgood. 1986. Chernical control of balsam twig aphid,
Mindams abieîinus Koch (Homoptera: Aphididae). Maine agncultural
experiment station. University of Maine. Technical bulletin 124.12 p.
Dixon, A.F.G. 1973. Biology of aphids. Edward Arnold (Publishers) Limited. London.
58 p.
Dunning, R.A., Baker, A.N. and R.F. Windley. 1975. Carabids in sugar beet crops
and their possible role as aphid predators. Ann. Appl. Biol. 80: 125-128.
Edwards. C.A.. Sunderland. K.D. and K.S. George. 1979. Studies on polyphagous
predators of cereal aphids. J. Appl. Ecol. 16: 81 1-823.
Hagen, K.S. and R. Van den Bosch. 1968. Impact of pathogens, parasites and
predators on aphids. Ann. Rev. Entomo!. 13: 325-384.
Hodek, 1. 1973. Biology of Coccinellidae. Academia. Prague Dr W. Junk. The
Haghe. 260 p.
Mensah, R.K. and J.L. Madden. 1994. Conservation of two predator species for
bioiogicai control of Chrysophthafta bimaculata (Coleoptera: Chrysomelidae)
in tasmanian forests. Entornophaga 39: 71-83.
Nettleton, WA. and F.P. Hain. 1982. The liie history, foliage darnage, and control of
the balsarn îwig aphid. Mindarus abietinus (Hornoptera: Aphididae), in fraser
fir Christmas tree plantations of western Norlh Carolina. Can. Entornol. 114:
155-1 65.
Pimentel, D. and A.G. Wheeler. 1973. Species diversity of arthropods in the alfalfa
cornmunity. Environ. Entomol. 2: 659668.
Rather, M. and N.J. Mills. 1989. Possibilities for the biological control of Christmas
tree pests, the balsam gall rnidge Pamdiplosis tumifex Gagné (Diptera:
Cecidornyiidae) and the balsam twig aphid, Mindams abietinus Koch
(Homoptera: Mindandae), using exotic enernies from Europe. Biocontrol
News and Information 19: 11 9-129.
Stary, P. 1995. Natural enemy spectrurn of Aphis spiraephaga (Hom: Aphididae), an
exotic immigrant aphid in central Europe. Entornophaga 40: 29-34.
Sunderland, K.D. and G.P. Vicketman. 1980. Aphid feeding by sorne polyphagous
predators in relation to aphid density in cereal fields. J. Appl. Ecol. 17: 389-
396.
Varty, I.W. 1966. The seasonal history and populaiion trends of the balsarn twig
aphid, Mindarus abietinus Koch, in New Brunswick Forest research
laboratory. Fredericton. 21 p.
Varty, I.W. 1968. The biology of the balsarn twig aphid, Mindarus abietinus Koch, in
New Brunswick: polyrnorphism, rates of developrnent, and seasonal
distribution of populations. Forest research laboratory. Fredericton. 65 p.
Vickenan. G.P. and K.D. Sunderland. 1975. Arihropods in cereal crops: nocturnal
activity, vertical distribution and aphid predation. J. Appl. Ecol. 12: 755-765.
White, RE. 1983. A field guide to the beetles on Norih America. Houghton Miiin
Company. Boston. 368 p.
Table 1 : Total captures of M. abietinus alates and P. rugosulus aduits in Malaise traps used in four commercial Christmas tree plantations near Sherbrooke, Québec, in 1996 and description of surrounding habitats
Locality Insecticides M. abietinus P. diaderna Surrounding habitats
Sawyerville Untreated 464 135 Forests East-Clifî on Untreated 1792 27 Agriculture fields Lennoxville Treated 49 O Agriculture fields Cookshire Treated 43 O Fields and forests
Figure 1: Seasonal trends in captures of P. rugosulus (Ntraplday) in Malaise traps
and M. abietinus alates (Ntraplday) with yellow sticky traps used in two
untreated commercial Christmas tree plantations near Shetbrooke (A and
B). Balsam twig aphid (Ntapex) and P. a go su lus (Ntree) densities in the
SawyeMlle plantation of balsam fir (C), Québec in 1996.
A) East-Clifton
A
2 40-. C) Sawyerville n
.- 2' 20.. -- 1
120 135 150 165 180 195 21 0
May June July Julian Days
Figure 2: Seasonal trends of Podabrus mgosulus behaviour (A) and distribution on
balsam fir trees (6) in a commercial Christmas tree plantation in Sawyerville,
Québec in 1996. Number of observations indicated above al1 columns.
Activities
Mating [7 Resting Moving [7 searching and predation
Thirds
Upper [7 Middle Lower
163 166 170 173 1TI 180 184
June Julian Days
187 191 194
July
Conclusion générale
La guilde des prédateurs attaquant le puceron des pousses du sapin en
plantations d'arbres de Noël est diversifiée, particulièrement chez les coccinelles
avec huit especes. Cependant, seulement deux d'entre elles ont montrées une
abondante suffisante en 1996 pour faire l'objet d'études en conditions naturelles et
ëtre considérées comme ayant un impact potentiel dans ce système. Les résultats
montrent que les coccinelles, particulièrement Anatis mali Say, sont les prédateurs
les plus hâtifs dans ce système et qu'elles sont capables d'attaquer les fondatrices
du puceron. Cette activité hâtive d'A. mali laisse entrevoir la possibilité qu'elle
pourrait limiter les dommages esthétiques aux arbres causés par les colonies de
pucerons issues de la reproduction des fondatrices. De plus, les adultes d'A. mali
sont également plus actifs que les adultes des autres espèces durant cette période
augmentant ainsi l'impact sur les fondatrices.
Une comparaison entre les deux especes dominantes de ce système montre
que la coccinelle indigène A. mal; est mieux adaptée au puceron des pousses du
sapin que la coccinelle exotique récemment introduite H axyndis. En effet, le
développement d'A. maliest mieux synchronisée avec celui de sa proie, montre une
plus grande efficacité de recherche, est plus rapide dans ses déplacements et
effectue plus souvent de la prédation. De plus, comme elle est une espèce indigène,
elle pourrait être climatiquement mieux adaptée ce qui lui permet d'être active plus
tôt dans la saison.
Les résultats obtenus indiquent une utilisation spatiale diiferente sur le sapin
baumier pour ces deux especes de coccinelles à l'exception des stades larvaires qui
doivent nécessairement tendre vers une distribution similaire puisqu'elles se
noumssent du même ravageur durant une courte période de temps. En effet, les
adultes (hivernants et nouveaux), les oeufs et les pupes sont distribués
différemment sur les arbres pour ces deux espèces. Pour H. axyridis la distribution
des stades est directement proportionnelle au volume de feuillage disponible dans
chacun des tiers de i'arbre (distribution aléatoire) ne démontrant ainsi aucune
préférence particulière. La distribution non aléatoire des différents stades de la
coccinelle A. mali indique qu'elle possède une préférence pour certaines portions
des arbres. Par exemple, les oeufs sont principalement déposés dans le tiers
inférieur des arbres facilitant probablement ainsi la prédation subséquente des
larves. Par ailleurs, la distribution des pupes sur les arbres diminue la mortalité de
ces demières chez A. mali.
Comme chez la majoriîé des coccinelles (Dixon 1970; Wright et Laing 1980;
Honek 1980; Evans et Dixon 1986), la ponte d'A. mali est mieux synchronisée avec
l'apparition des colonies de pucerons sur les arbres et les larves arrivent durant la
période ou la ressource alimentaire est la plus abondante contrairement aux larves
d'H. axynds qui arrivent majoritairement lots de la dispersion du ravageur. De plus.
i'activité prédatrice et la vitesse de déplacement des larves de la coccinelle A. mali
sont supérieures à celle d'H axyndis. Selon Dixon (1959, 1970) et Carter et Dixon
(1 984), ces qualités influencent directement l'impact que peuvent avoir les l a ~ e s sur
les niveaux de populations du ravageur.
D'autre part, il existe à l'état naturel une relation de prédation intraguilde (IGP)
(Evans 1991 ; Polis et a. 1989; Rosenheim et 4.1995) entre ces deux espèces de
coccinelles. La coccinelle A. mali est particulièrement agressive, même contre les
individus de sa propre espéce (cannibalisme) (Gagné et Martin 1968). Durant le
développement larvaire, la relation de prédation intraguilde est unidirecîionnelle en
faveur de la coccinelle A. mali. L'éclosion hâtive des larves de la coccinelle A. mali et
leur taille supérieure pour un stade donné avantage ces demières dans leur relation
intraguilde avec les larves d'H. axyndis. Cependant, au cours de son dernier stade
larvaire. la coccinelle H. axyndis peut être, comme A. mali, un prédateur intraguilde
des prépupes et des pupes de l'autre espèce de coccinelles.
Les deux espèces de coccinelles ont réussi à augmenter leurs populations
respectives durant le cycle du puceron des pousses du sapin, A. mali par un facteur
de 13 comparativement à 5 pour H. axyridis. Ce.s résultats indiquent que la
coccinelle A. mali a davantage profité des densités épidémiques du puceron des
pousses du sapin en 1996 et a ainsi pu accroître de manière plus importante sa
population que la coccinelle exotique H. axyndis.
Le système du puceron des pousses du sapin en plantations d'arbres de
Noël a permis d'investiguer l'impact des larves de coccinelles puisque la période
d'oviposition des coccinelles est de courte durée. II est ainsi possible, avec la
technique d'exclusion manuelle (Luck et a. 1988; Jervis et Kidd 1996), d'éliminer les
masses d'oeufs de coccinelles pondus sur les arbres. Cette opération permet
d'obtenir des arbres dépourvus de prédation exercée par les larves de coccinelles et
ainsi la possibilité d'évaluer leur impact sur les populations de pucerons (Jervis et
Kidd 1996). Cette expérimentation est donc innovatrice puisqu'elle permet pour la
première fois d'évaluer, sur le terrain l'impact réel de la prédation exercée par les
larves de coccinelles.
L'impact de la prédation exercée par les l a ~ e s de coccinelles sur les densités
du puceron des pousses du sapin est important. Les larves de coccinelles diminuent
de manière significative la densité des colonies du puceron sur les arbres. De plus,
la densité des pucerons dans les colonies restantes est également diminuée de
façon substantielle par l'action prédatrice des larves. Cette double situation entraine
donc une diminution des densités de pucerons sur les arbres lorsqu'il y a présence
de larves de coccinelles. La prédation des larves de coccinelles a entrainé une
diminution significative des densités d'oeufs hivernants du puceron des pousses du
sapin. Cette diminution devrait entraîner des densités initiales de fondatrices
moindres et par le fait même des niveaux d'infestations inférieurs l'année suivante.
Cependant, la prédation des larves de coccinelles est incapable de diminuer
le pourcentage de pousses endommagées sur les arbres puisqu'elle est intervient
après le début de la formation des colonies dont dépendent les dommages
esthétiques. Leur action prédatrice semble toutefois diminuer l'intensité des
dommages (N aiguilles croches/ pousse) sur les pousses annuelles. Par ailleurs,
leur présence sur les arbres a un effet bénéfique pour la plante hôte qui se traduit
par une meilleure croissance élongative des pousses annuelles. Comme le montre
les récents travaux de Desrosiers (1998). le puceron des pousses du sapin affecte
la croissance en hauteur des sapins. La diminution des densitéç du puceron sur les
arbres causée par l'action prédatrice des larves de coccinelles n'a cependant pas
été assez importante pour influencer significativement cette variable.
La voracité des larves de coccinelles est le principal facteur déterminant leur
efficacité (Gumey et Hussey 1970; Mills 1982). L'espèce dominante de ce système,
la coccinelle A. mali. possède une voracité importante si on la compare à Mulsantina
hudsonica Casey (Varty 1969). En effet, durant son développement larvaire cette
coccinelle consomme en moyenne 269 pucerons des pousses du sapin de
quatrième stade ou adulte de la deuxième génération. Cette consommation est 8.5
fois supérieure à celle de M .hudsonica élevé sur le même stade de puceron (Va*
1969). Lorsqu'exprimé en nombre de colonies, cette voracité représente un
minimum de sept colonies consommées par larve en fonction de la densité
moyenne rencontrée dans les colonies en 1996.
En plus des prédateurs habituels des pucerons (coccinelles, syrphides et
chiysopes), une espèce prédatke du puceron des pousses du sapin a été identifiée
pour la première fois. II s'agit de Podabnis mgosulus Leconte une espece de
Cantharidae (Coléoptère). Cette espece est surtout active lors de la dispersion du
ravageur, et elle ne peut donc prévenir l'apparition des dommages esthétiques sur
les arbres. La découverte de P. nigosulus ainsi que le relevé des prédateurs
naturels montrent que la diversité des prédateus attaquant le puceron des pousses
du sapin au Québec est importante lorsque les traitements insecticides n'interfèrent
pas avec leur action et leur survie.
La guilde des prédateurs attaquant le puceron des pousses du sapin est
diversifiée et leur action prédatrice, particulièrement les larves de coccinelles, peut
diminuer les niveaux de populations de ce ravageur. Cependant, d'autres
recherches sont nécessaire pour accroître nos connaiçsances sur ce sujet. Des
investigations sont nécessaires pour déteminer les lieux d'hivemement et la
mortalité hivernale des especes dominantes de coccinelles, ce qui pemett& de
mieux prévoir le retour des coccinelles lors des saisons subséquentes. Par ailleurs,
l'impact des coccinelles adultes, principalement A. mali, sur les densités des
fondatrices devrait être examiné afin de connaître leur impact sur le développement
des infestations de ce ravageur.
L'importance du couvert forestier adjacent aux plantations d'arbres de Noël
devrait ëtre examinée puisque le couvert forestier influence directement la diversité
des especes de même que leur date d'arrivée dans un habitat particulier (Honek
1985; Hodek et Honek 1996). Pour la coccinelle A. mali, l'importance des conifères,
particulièrement le pin rouge, devrait également être vérifiée puisque nos données
fragmentaires indique que cette essence semble jouer un rôle de premier plan pour
cette coccinelle indigène. Les travaux de Gagné et Martin (1968) laissent également
supposer une étroite relation entre cette essence et cette coccinelle. L'utilisation
d'attractants peut être envisagée pour attirer les coccinelles plus hâtiv&nent dans
les plantations. Certains travaux ont déjà montré l'efficacité de cette technique
(Ewert et Chiang 1966; Schiefelbein et Chiang 1966; Ben Saad et Bishop 1976;
Mensah et Madden 1994). Des suppléments alimentaires pour permettre une
maturation plus rapide des oocytes des coccinelles et donc une ponte plus hâtive
peuvent également être envisagés. Lorsque les différentes composantes du cycle
vital des coccinelles seront connues, il pourrait s'avérer possible de modifier
adéquatement i'habiiat pour les rendre plus efficaces contre le puceron des pousses
du sapin et ainsi limiter les effets négatifs de ce ravageur.
Références bibliographiques
Agarwala, B.K. and A.F.G. Dixon. 1992. Laboratory study of cannibalism and
interspecific predation in ladybirds. Ecol. Entomol. 17: 303-309.
Amman, G.D. 1963. A new distribution record for the balsarn twig aphid. J. Econ.
Entomol. 56: 11 3.
Andow, D.A. and S.J. Risch. 1985. Predation in diversified agroecosystems: relation
between a coccinellid predator Coleomegilla maculata and its food. J. Appl.
Ecol. 22: 357-372.
Arnett, R.H. 1963. The beetles of the United States (a manual for identification). The
catholic university of America Press. Washington. 11 12 p.
Arnold, T.B. and D.A. Potter. 1987. Impact of a high-maintenance lawncares
program on nontarget invertebrates in Kentucky bluegrass turf. Environ.
Entomol. 16: 100-105.
Banks, C.J. 1956. Observations on the behavior and mortality in coccinellidae before
dispersal from the egg shells. Proc. Roy. Entomol. Soc. London. A 31: 56-
60.
Bellows. T.S., Van Dnesche, R.G. and J.S. Elkinton. 1992. Life-table construction
and analysis in the evaluation of natural enemies. Ann. Rev. Entomol. 37:
587-614.
Ben Saad. A.A. and G.W. Bishop. 1976. Attraction of insects to potato plants
through use of artificial honeydews and aphid juice. Entomophaga 21: 49-
57.
Bradbury, R.L. and EA. Osgood. 1986. Chernical control of balsam twig aphid,
Mindams abietinus Koch (Hornoptera: Aphididae). Maine agricultural
experirnent station. Univers.ky of Maine. Technical bulletin 124, 12 p.
Campbell, C.A.M. and W.W. Cone. 1994. Influence of predators on population
development of Phomdon humili (Hornoptera: Aphididae) on hops. Environ.
Entornol. 23: 1391-1396.
Carter. M.C. and A.F.G. Dixon. 1982. Habitat quality and the foraging behaviour of
coccinellid larvae. J. Anirn. Ecol. 51: 865-878.
Carter, M.C. and A.F.G. Dixon. 1984. Foraging behaviour of coccinellid iarvae:
duration of intensive search. Entornol. exp. appl. 36: 133-136.
Cloutier, C. and C. Cloutier. 1992. Les solutions biologiques de lutte pour la
répression des insectes et acariens ravageurs des cultures. Dans Vincent
C. et D. Coderre (Eds.). La lutte biologique. Gaëtan Morin Editeur. Montréal.
pp. 19-88.
Cockfield, S.D. and D.A. Potter. 1983. Short-term effects of insecticidal applications
on predaceous arthropods and oribatid mites in Kentucky bluegrass turf.
Environ. Entornol. 12: 1260-1264.
Coderre D. and J.C. Tourneur. 1986. Vertical distribution of aphids and
aphidophagous insects on rnaize. In: Hodek, 1. (ed.): Ecology of
aphidophaga. Academia. Prague & Dr. W. Junk. Dordrecht. pp. 291-296.
Coderre, D., Provencher, L. and J.C. Tourneur. 1987. Oviposition and niche
partitioning in aphidophagous insectç on rnaize. Can. Entornol. 119: 195-
203.
Coderre, D.. Provencher, L. and J. Champagne. 1989. Effect of intercropping maize-
beans on aphids and aphidophagous insects in corn fields of southern
Québec, Canada. Acta Phytopathologica et Entornologica Hungarica 24: 59-
63.
Coderre, D., Lucas, E. and 1. Gagné 1995. The occurence of Harmonia axyridis
(Pallas) (Coleoptera: Coccinellidae) in Canada. Can. Entomol. 127: 609-
611.
Coll, M. and R.L. Ridgway. 1995. Functional and numencal responses of Orius
insidiosus (Heteroptera: Anthocoridae) to its prey in different vegetal crops.
Ann. Entomol. Soc. Am. 88: 732-738.
DeBach, P. 1974. Biological control by natural enernies. Cambridge. University
Press. 323 p.
Deland. J.-P., Berthiaurne, R., Hébert, C. and C. Cloutier. 1998. Programme
alternatif de protection du sapin de Noël contre le puceron des pousses du
sapin dans le contexte d'une saine gestion des ressources
environnementales. Rapport final 1998. Projet de recherche et technologie
en environnemEntorno1. Ministère de l'environnement et de la faune.
Québec. 105 p.
Desrosiers, N. 1998. Influence de la fertilisation azotée et de la date de
débourrement sur les populations du puceron des pousses du sapin,
Mindarus abietinus Koch. (Homoptère: Aphididae). Mémoire de maîtrise.
Département de biologie. Université Laval. Québec. 109 p.
Dixon, A.F.G. 1959. An expenrnental study of the searching behavior of the
predatory coccinellid beetle Adalia decempunctata (L). J. Anirn. Ecol. 28:
259-281.
Dixon, A.F.G. 1970. Factors lirniting the effectiveness of the coccinellid beetle,
Adalia bipunctata (L.) as a predator of the sycarnore aphid, Drepanosiphum
platanoides (Schr.). Anim. Ecol. 39: 739-751.
Dixon, A.F.G. 1973. Biology of aphids. Edward Arnold (Publishers) Lirnited. London.
58 p.
Dreistadt, S.H. and M.L. Flint. 1996. Melon aphid (Hornoptera: Aphididae) control by
inundative convergent lady beetle (Coleoptera: Coccinellidae) release on
Chrysanthernurn. Environ. Entornol. 25: 688-697.
Dunning. RA., Baker. A.N. and R.F. Windley. 1975. Carabids in sugar beet crops
and their possible role as aphid predators. Ann. Appl. Biol. 80: 125-128.
Edwards, C.A., Sunderland, K.D. and K.S. George. 1979. Studies on polyphagous
predators of cereal aphids. J. Appl. Ecol. 16: 81 1-823.
Ehler, L.E. and J.C. Miller. 1978. Biological control in temporary agroecosysterns.
Entornophaga 23: 207-212.
Elliott, N.C. and R.W. Kieckhefer. 1990. Dynarnics of aphidophagous coccinellid
assemblages in srnall grain fields in eatern south Dakota. Environ. Entornol.
19: 1320-1329.
Elliott. N.C., Kieckhefer, R.W. and W. Kauffrnan. 1996. Effects of an invading
coccinellid on native coccinellid in an agricultural landscape. Oecologia 105:
537-544.
Evans, E.W. 1991. lntra versus interspecific interactions of ladybeetles (Coleoptera:
Coccinellidae) attacking aphids. Oecologia 87: 401408.
Evans, E.W. and A.F.G. Dixon. 1986. Cues for oviposition by ladybird beetles
(Coccinellidae): response to aphids. J. Anirn. Ecol. 55: 1027-1034.
Ewert, M.A. and H.C. Chiang. 1966. Dispersal of three species of coccinellids in corn
fields. Can. Entornol. 98: 999-1003.
Fox, L.R. 1975. Cannibalism in natural populations. Ann. Rev. Ecol. Syst. 6: 87-106.
Frazer. B.D. and B. Gill. 1981. Hunger, movement, and predation of Coccinella
califomica on pea aphids in the laboratory and in the field. Can. Entornol.
1 13: 1025-1 033.
Frazer, B.D., Gilbert, N., Ives, P.M. and D.A. Raworth, 1981. Predator reproduction
and the overall predator-prey relationship. Can. Entomol. 11 3: 101 5-1 024.
Gagné, W.C. and J.L. Martin. 1968. The insect ecology of red pine plantations in
central Ontario. Can. Entornol. 100: 835-846.
Gawande, R.B. 1966. Effect of constant and alterning temperatures on feeding and
developrnent of Chilomenes sexmaculata Fb. In Hodek, 1. (ed): Ecology of
aphidophagous insects. Acadernia. Prague & Dr W. Junk. The Hague. pp.
63-67.
Gumey, B. and N.W. Hussey. 1970. Evaluation of sorne coccinellid species for the
biological control of aphids in protected cropping. Ann. Appl. Biol. 65: 451-
458.
Hagen, K.S. 1 9 0 . Biology and ecology of predaceous coccinellidae. Ann. Rev.
Entomol. 7: 289-326.
Hagen, K.S. and R. van den Bosch. 1968. Impact of pathogens, parasites and
predators on aphids. Ann. Rev. Entomol. 13: 325-384.
Hams, J.W.E. and W.W. Bowers. 1995. Insectes forestiers ravageurs au Canada.
Ministère sciences naturelles. Ottawa. 843 p.
Hodek, 1. 1967. Bionomics and ecology of predaceous Coccinellidae. Ann. Rev.
Entornol. 12: 79-1 04.
Hodek, 1. 1970. Coccinellids and the modem pest management. Biosciences 20:
543-552.
Hodek. 1. 1973. Biology of Coccinellidae. Academia. Prague Dr W. Junk. The
Haghe. 260 p.
Hodek. 1. 1993. Habitat and food specificity in aphidophagous predators (a review).
Biocontrol Sci. Technol. 3: 91-100.
Hodek, 1. and A. Honek 1996. Ecology of Coccinellidae. Kluwer academic
publishers. Boston. 464 p.
Hoelrner, K.A.. Osbome, L.S. and R.K. Yokomi. 1993. Reproduction and feeding
behavior of Delphastus pusillus (Coleoptera: Coccinellidae), a predator of
Bemisia tabaci (Hornoptera: Aleyrodidae). J. Econ. Entornol. 86: 322-329.
Honek, A. 1980. Population density of aphid at the tirne of seitling and ovanole
maturation in Coccinella septempunctata (Coleoptera. Coccinellidae).
Entomophaga 25: 427-430.
Honek, A. 1985. Habitat preferences of aphidophagous coccinellids (Coleoptera).
Entornophaga 30: 253-264.
Howarth, F.G. 1991. Environmental impacts of classical biological control. Ann. Rev.
Entornol. 36: 485-509.
lablokoff-Khnzorian, S.M. 1982. Les coccinelles (Coléoptères- Coccinellidae) des
régions paléartique et onentale. Editions Boubée. Pans. 586 p.
Iperti, G. 1966. Comportement naturel des coccinelles aphidiphages du sud-est de
la France: leur type de spécificité. leur action prédatrice sur Aphis fabae L..
Entomophaga 2: 203-210.
Iperii, G. and S. Quillici. 1986. Some factors influencing the selection of oviposition
site by Propylea quatuordecimpunctata. In: Hodek, 1. (ed.): Ecology of
aphidophaga. Academia. Prague & Dr. W. Junk. Dordrecht. pp. 137-142.
Ives, P.M. 1981. Feeding and egg production of iwo species of coccinellids in the
laboratory. Can. Entomol. 113: 999-1 005.
Jewis, M. and N. Kidd. 1996. lnsect natural enernies: practical approaches to their
study and evaluation. Chapman 8 Hall. London. 491 p.
Kairo, M.T.K. and S.T. Murphy. 1995. The life histoiy of Rodolia iceryae Janson
(Col., Coccinellidae) and the potential for use in innoculative releases
against lcerya pattersoni Newstead (Hom., Margarodidae) on coffee. J.
Appl. Entomol. 11 9: 487491.
Kesten. V.U. 1969. Zur morphologie und biologie von Anatis ocellata (L.)
(Coleoptera: Coccinellidae). Z Angew. Entomol. 63: 412-455.
Kieckhefer. R.W. and N.C. Elliott. 1990. A 13-year survey of the aphidophagous
coccinellidae in maize fields in eastem south Dakota. Can. Entomol. 122:
579-581.
Kieckhefer, R.W. and B.H. Kantack. 1980. Loses in yield in spring wheat in South
Dakota caused by cereal aphids. J. Econ. Entomol. 31: 455478.
Kirby, K.N. 1993. Advanced data analysis with SYSTAT. Van Nostrand Reinhold CO.
New York. 475 p.
Kleintjes, P.K. 1997. Midseaçon insecticide treatment of balsam twig aphids
(Homoptera: Aphididae) and their aphidophagous predators in a Wisconsin
Christmas tree plantation. Environ. Entomol. 26: 1393-1397.
Kring, T.J.. Gilstrap, F.E. and G.J. Michels. 1985. Role of indigenous coccinellids in
regulating greenbugs (Homoptera: Aphididae) on Texas grain sorghum. J.
Econ. Entomol. 78: 269-273.
Kuno, E. 1991. Sarnpling and analysis of insect populations. Ann. Rev. Entomol. 36:
285-304.
Lapchin, L., Ferran, A., Iperti, G., Rabasse, J.M. and J.P. Lyon. 1987. Coccinellids
(Coleoptera: Coccinellidae) and syrphyds (Diptera: Syrphidae) as predators
of aphids in cereal crops: a cornpanson of sampling methods. Can.
Entornol. 119: 815-822.
Luck. R.F., Shepard, B.M. and P.E. Kenrnore. 1988. Experirnental rnethods for
evaluating arthropod natural enernies. Ann. Rev. Entornol. 33: 361-391.
McMullen, R.D. 1967. A field study of diapause in Coccinella novemnotata
(Coleoptera: Coccinellidae). Can. Entomol. 99: 42-49.
Mensah, R.K. and J.L. Madden. 1994. Conse~ation of two predator species for
biological control of Chrysophtharta bimaculata (Coleoptera: Chrysornelidae)
in Tasrnanian forests. Entornophaga 39: 71 -83.
Mills, N.J. 1982. Voracity, cannibalisrn and coccinellid predation. Ann. Appl. Biol.
101: 144-148.
Murdoch, W.W. 1973. The functional response of predators. J. Appl. Ecol. 10: 335-
342.
Nettleton, W.A. and F.P. Hain. 1982. The life history, foliage darnage, and control of
the balsarn twig aphid, Mindams abietinus (Hornoptera: Aphididae), in fraser
fir Christmas tree plantations of wesiern North Carolina. Can. Entornol. 114:
155-1 65.
Ng, S.M. 1986. The geotactic and phototactic responses of four species of
aphidophagous coccinellid lawae. In: Hodek, 1. (ed.): Ecology of
aphidophaga. Acadernia. Prague & Dr. W. Junk Dordrecht. pp. 57-68.
Obata, S. 1986. Mechanisrns of prey finding in the aphidophagous ladybird beetle.
Harmonia axynüis (Coleoptera: Coccinellidae). Entornophaga 31 : 303-31 1.
Obata S., Johki, Y. and T. Hidaka. 1986. Location of hibernation sites in the ladybird
beetle, Harmonia axyridis. ln: Hodek, 1. (ed.): Ecology of aphidophaga.
Acadernia. Prague & Dr. W. Junk Dordrecht. pp. 193-198.
Obrycki, J.J. and M.J. Tauber. 1981. Phenology of three coccinellid species: thermal
requirements for development. Ann. Entornol. Soc. Am. 74: 31-36.
Ongagna, P. and G. Iperti. 1994. Influence de la température et de la photopériode
chez Harmonia axynds Pall. (Col., Coccinellidae): obtention d'adultes
rapidement féconds ou en dormance. J. Appl. Entornol. 117: 314-317.
Osawa, N. 1989. Sibling and non-sibling cannibalisrn by lame of a lady beetle
Harmonia axyndis Pallas. (Coleoptera: Coccinellidae) in the field. Res.
Popul. Ecol. 31: 153-160.
Pirnentel, D. and A.G. Wheeler. 1973. Species diversity of arthropods in the alfalfa
cornrnunity. Environ. Entornol. 2: 659-668.
Polis, G.A. 1981. The evolution and dynarnics of intraspecific predation. Ann. Rev.
EcoI. Syst. 12: 225-251.
Polis, G.A., Myers, CA. and R.D. Holt. 1989. The ecology and evolution of intraguild
predation: potential cornpetitors that eat each other. Ann. Rev. Ecol. Syst.
20: 297-330.
Rather, M. and N.J. Mills. 1989. Possibiliiies for the biological control of Christmas
tree pests, the balsarn gall rnidge Paradiplosis tumifex Gagné (Diptera:
Cecidornyiidae) and the balsarn twig aphid, Mindams abietinus Koch
(Hornoptera: Mindaridae), using exotic enernies frorn Europe. Biocontrol
News and Information 19: 119-129.
Reinert, J.A. 1978. Natural ennerny cornplex of the southem chirig bug in Florida.
Ann. Entornol. Soc. Am. 71: 726-731.
Renault, T. 1983. Puceron des pousses du sapin et cécidornyie du sapin (shation-
1983). Centre de recherches forestières des maritimes. Note technique No
8OF. 9 p.
Reyd, G. and B. Le RU. 1992. Impact of predation by coccinellid lawae on colonies
of the rnealybug Phenacoccus manihoti in crops lands. Acta Oecologica 13:
181-191.
Rice, M.E. and G.E. Wilde. 1988. Experirnental evaluation of predators and
parasitoids in suppressing greenbugs (Hornoptera: Aphididae) in sorghurn
and wheat. Environ. Entornol. 17: 836-841.
Roger, C.. Coderre, D. and C.VincEntornol. 1994. Mortal i and predation of
Coleomegilla maculata lengi (Coleoptera: Coccinellidae) following pesticide
applications. J. Econ. Entornol. 87: 583-588.
Rondeau, G. and J.L. DesGranges. 1991. Effets des arrosages du diaUnon
(basudin), du diméthoate (cygon) et su savon insecticide (safer trn) sur la
faune avienne dans les plantations de sapins de noël. Service canadien de
la faune. Région de Québec. Série de rappotts techniques No 141.54 p.
Rose A.H. and O.H. Lindquist. 1994. Insectes des epinetîes, du sapin et de la
pruche de I'est du Canada. Reçssources naturelles Canada. Ottawa. 159 p.
Rosenheim, J.A., Kaya, H.K., Ehler, LE., Marois. J.J. and BA. Jaffee. 1995.
lntraguild predation among biological control agents: theory and evidence.
Biological control5: 303-335.
Rosenzweig, M.L. 1981. A theory of habitat selection. Ecology 62: 327-335.
Schiefelbein. J.W. and H.C. Chiang. 1966. Effects of spray of sucrose solution in a
corn field on the populations of predatory insects and their prey.
Entomophaga 11 : 333-339.
Simberloff, D. and P. Stiling. 1996. How nsky is biological control. Ecology 7: 1965-
1974.
Smith, B.C. 1965a. Differences in Anatis mali Auct. and Coleomegilla maculata lengi
Timberlake to changes in the qualii and quantity of the lawal food
(Coleoptera: Coccinellidae). Can. Entomol. 97: 1159-1 166.
Smith, B.C. 1965b. Growth and development of coccinellid larvae on dry foods
(Coleoptera: Coccinellidae). Can. Entomol. 97: 760-768.
Smith, C.C., Newell, W.R. and T.R. Renault. 1981. Common insects and diseases
of balsam fir Christmas trees. Canadian Forestty Service. Technical Note.
No 1328.63 p.
Spence, J.R. and H.E. Carcamo. 1991. Effects of cannibalism and intraguild
preoation on pondskaten (Gemdae). Oikos 62: 333-341.
Snyder, W.E. and L.E. Hurd. 1995. Egg-hatch phenology and intraguild predation
between two mantid specisç. Oecologia 104: 496-500.
Stary, P. 1975. Pseudopraon mindanphagum gen. n., sp. n. (Hymenoptera:
Aphidiidae), Description and life history of a parasite of Mindarus abietinus
(Homoptera: Mindaridae) in central Europe. Acta. Entomol. Bohemoslov. 72:
249-258.
Stary, P. 1995. Natural enemy spectrum of Aphis spiraephaga (Hom: Aphididae), an
exotic immigrant aphid in central Europe. Entomophaga 40: 29-34.
Sunderland, K.D. and G.P. Vicketman. 1980. Aphid feeding by some polyphagous
predaton in relation to aphid density in cereal fields. J. Appl. Ecol. 17: 389-
396.
Tamaki, G.. Annis, B., and M. Weiss. 1981. Response of natural enemies to the
green peach aphid in different plant cultures. Environ. Entomol. 10: 375-
378.
Van Driesche, R.G. and T.S. Bellows. 1996. Biological control. Chapman et Hall.
New York. 539 p.
Varty, I.W. 1966. The seasonai history and population trends of the balsam twig
aphid, Mindams abietinus Koch, in New Brunswick. Forest research
laboratory. Fredericton. 21 p.
Varty, I.W. 1968. The biology of the balsam twig aphid, Mindarus abietinus Koch, in
New Brunswick: poiymorphism. rates of development, and seasonal
distribution of populations. Forest research laboratory. Fredericton. 65 p.
Varty. LW. 1969. Ecology of Mulsantina hudsonica Casey, a ladybeetle in fir-sp~ce
forest, Forest research laboratory. Fredericton, 28 p.
Vickerrnan G.P. and K.D. Sunderland. 1975. Arthropods in cereal crops: nocturnal
activity, vertical distribution and aphid predation. J. Appl. Ecol. 12: 755-765.
Watson. W.Y. 1976. A review of the genus Anatis Mulsant (Coleoptera:
Coccinellidae). Can. Entornol. 108: 935-944.
Wissinger, S.A. 1997. Cyclic colonization in predictably epherneral habitats: a
template for biological control in annual crop systerns. Biological Control 10:
4-1 5.
White, R.E. 1983. A field guide to the beetles on North America. Houghton Mifflin
Company. Boston. 368 p.
Wright, E.J. and J.E. Laing. 1980. Nurnencal response of coccinellids to aphids in
com in southern Ontario. Can. Entornol. 112: 977-988.
Wright, D.J. and R.H.J. Verkerk. 1995. lntegration of chernical and biological control
systems for arthropods: evaluation in a multitrophic context. Pesiic. Sci. 44:
207-21 8.
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