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Defense Strategies ofFolivorous Sawflies
Sylvio G. Codella, Jr.Kenneth F. RaffaDepartments of Entomology and ForestryUniversity of Wisconsin-MadisonMadison, Wisconsin
I. IntroductionII. Predators 01 Sawflies
A. ArthropodsB. Vertebrates
Ill. Escape in Time and SpaceIV. Physical DelensesV. Chemical Delenses
A. Modes 01 Storage and DeliveryB. Sources and Composition 01 AJlomonesC. Development and Behavior in Relation to Chemical Defense
VI. Camouflage, Aposematism, and MimicryVII. Gregarious Behavior: Multiple Selection Pressures?
A. DiseaseB. DevelopmentC. Predation
VIII. Conclusions and ProspectsReferences
A fundamental goal of evolutionary biology is to explain the existence ofapparently adaptive traits (Mayr, 1983). In this regard, antipredator charac-ters have received considerable attention, and their study has contributedsubstantially to the development of evolutionary theory (Fisher, 1930).Indeed, the effects of predation are "uniquely c1earcut" (Curio, 1976) andare therefore expected to result in strong selection for defensive adapta-tions (Heads and Lawton, 1985 Lima and Dill, 1990). Likewise, studies canalso help us place predation in its proper ecological context (Endler, 1986).
Present address: Department of Biology, Northland College, Ashland, Wisconsin.
SowRy Life History AdoplOflons to Woody PlantsCopyright 1993 by Academic Press. Inc. All rights of reproduction in any form reserved. 261
262 Sylvia G. Codella, Jr. and Kenneth F. Raffa
It remains a major challenge to biologists to define the conditions that favorthe evolution of particular modes of defense and to explore the variousconstraints that may oppose their development (Harvey and Greenwood,1978; Pasteels et al., 1983).
Despite the impressive diversity of antipredator traits and the intuitiveappeal of the associated adaptive scenarios (see many examples in Cott,1940; Wickler, 1968; Edmunds, 1974; Blum, 1981; Pasteur, 1982; Evans andSchmidt, 1990), our knowledge in most cases has not extended beyond thedescriptive phase (Endler, 1986). As a result, we understand only the defen-sive potential (sensu Honda, 1983) of many characters and thus lack theability to integrate such traits into the overaJl picture of an organism's lifehistory strategy. Likewise, we possess a poor understanding of the costsassociated with defense (Harvey and Greenwood, 1978; Blum, 1981; Bowers,1989). As a result, defense strategies have rarely been incorporated intomodels of predator-prey population dynamics (Holling, 1965; Ives andDobson, 1987), despite their potentially profound effect on the behavior ofmany systems.
As the other chapters in this volume indicate, the study of sawflies cancontribute much to our understanding of evolution and comparative biol-ogy. As phytophagous hymenopterans, they are in a unique situation to becompared both to well-studied herbivorous insects with similar life-styles(e.g., many lepidopterans) and to their own parasitic and eusocial relatives.Despite intense attention from economic entomologists over many years,sawflies are still relatively understudied, and a great deal of interestinginformation has not yet found its way into the general biological literature.
We believe that defensive ecology is a case in point. For example,beyond several landmark papers (Prop, 1960; Eisner et al., 1974; morerecently, Bjorkman and Larsson, 1991), the well-known defensive regurgita-tion behavior of the Diprionidae has received little sustained attention.Putative defenses in other taxa have fared even worse. The goals of thischapter are to review a scattered literature, to identify understudied areasof promise, and to encourage additional work on sawfly defenses. Forreasons of space, we will focus primarily on the conifer sawflies (Diprio-nidae) but will also include discussion of other free-living, woody-plant-feeding families. Likewise, we will primarily concentrate on interactionswith predators rather than parasites (see Raizenne, 1957; Finlayson, 1963;and others for extensive catalogs of symphytan parasites). However, webelieve that many of these phenomena are applicable to both cases.
II. Predators of Sawflies
There are numerous published reports of naturally occurring (i.e., nonex-perimental) predation on sawflies. Many of these records are widely scat-
10 Defense trategies of Folivorous awfties 263
tered in the economic literature and are often anecdotal in nature. Thepredators involved possess a diversity of characteristics, such as searchbehavior, sensory capacity, and social organization, that could favor differ-ent prey defense strategies (Holling, 1958; Pasteels et al., 1983; Endler, 1990;Guilford, 1990).
Table 10.1 lists publications that mention arthropod predators of which weare aware. This list is not complete, and the number of citations for aparticular predator taxon does not necessarily reflect the frequency of aninteraction in nature. The table does, however, confirm that all stages ofsawflies are attacked by a variety of arthropod predators under naturalconditions (thus avoiding some of the controversies concerning selectiveagents on butterfly coloration; e.g., Marshall, 1909; Wheeler, 1935; Wourmsand Wasserman, 1985).
Surp.risingly, hymenopterans are among the most frequent prey itemsof predaceous terrestrial insects (Schoenly, 1990). At least 22 families in 12arthropod orders include species that prey on sawflies under natural condi-tions (Table 10.1). The majority of reports involve insects, but spider pre-dation also appears to occur with some frequency.
Arthropods attack all sawfly life stages. Most reports concern larvalpredation, although this may be due to the relative conspicuousness ofthat stage. Both empirical and anecdotal reports suggest that larval pre-dation has little influence on sawfly population dynamics (Morris et al.,1963; Carne, 1969; Olofsson, 1987). This may be a consequence of anti-predator traits. Tinbergen (1960) noted that sawfly larvae were abun-dant in Dutch forests yet were not utilized to any great degree by theavian fauna. Prop (1960) hypothesized that this was due to various defen-sive traits and provided the first detailed study of sawfly antipredator be-havior.
Two arthropod predators have been recorded with particular fre-quency. Among the Hemiptera, pentatomids, especially Podisus spp., appearto interact frequently with diprionids (Table 10.1). Reports of larval attacksare most common, but predation on the remaining life stages has also beenobserved. Tostowaryk (1971 b) described the life history and biology ofPodisus modestus. First-instar nymphs do not feed, but later instars requireprotein for growth. Nymphs agressively persist in attacks on Neodiprionspp. and at times appear to cooperate in killing and feeding (Tostowaryk,1971a). They often congregate near sawfly colonies. In contrast, adults feedless extensively and are less agressive.
Ant predation on sawflies has been observed frequently over manyyears (Table 10.1), resulting in several attempts to control pest populationswith transplanted colonies (Bradley, 1972; Williamson, 1973; Finnegan,1975). Attacks on larval colonies are frequently reported. Females are
264 Sylvia G. Codella, Jr. and Kenneth F. Raffa
TABLE 10.1 Arthropod Predators of Sawflies
Predator Prey StageQ Representative references
Oxyopidae DiprionidaeNeodiprion L Kapler and Benjamin, 1960
Thomisidae DiprionidaeDiprion L Coppel el al., 1974
Unspecified DiprionidaeDiprion A Coppel el al., 1974Neodiprion E Lyons, 1964
L Hetrick, 1959; Dahlsten, 1961; Lyons,1964; Pschorn-Walcher, 1965
A Hetrick, 1941; Coppel and Benjamin,1965
Prisliphora E Turnock, 1953Diprionidae
Neodiprion E Lyons, 1964Diplopoda
Unspecified DiprionidaeUnspecified C Coppel and Benjamin, 1965
Unspecified PamphiliidaeNeuroloma A Benson, 1950
DiprionidaeDiprion A Coppel el al., 1974Unspecified A Coppel and Benjamin, 1965
Diprion E Sturm, 1942Hemiptera
Pentatomidae TenthredinidaePrisliphora L Tostowaryk,1971aMonoslegia L Tostowaryk,1971a
DiprionidaeDiprion L Coppel and Benjamin, 1965
C Coppel el al., 1974Neodiprion E Benson, 1950; Wilkinson el al., 1966
L Benjamin el al., 1955; Benson, 1950;Kapler and Benjamin, 1960; Knererand Wilkinson, 1990; Lyons, 1964;Morris el al., 1963; Tostowaryk,1971a; Wilkinson et al., 1966
A Hetrick, 1959; Kapler and Benjamin,1960
Miridae DiprionidaeNeodiprion E Wilkinson et al., 1966; Smirnoff, 1959
TABLE 10.1 (Continued)
10 Defense tralegies of Folivorous Sawflies 265
Predator Prey StageQ Representative references
Nabidae DiprionidaeDiprion E Coppel et aI., 1974Neodiprion L Lyons, 1964; Coppel and Benjamin,
Diprion L Coppel et al., 1974Neodiprion L Knerer and Wilkinson, 1990; Lyons,
1964; Morris et al., 1963A Hetrick, 1959
Cimicidae TenthredinidaeNematus E Benson, 1950
Nematus E,L Benson, 1950Neuroptera
Chrysopidae PamphiliidaeNeurotoma L Benson, 1950
ArgidaeArga L Benson, 1950
DiprionidaeNeodiprion E Kolomeits et al., 1972; Lyons, 1964
Rhaphidiidae DiprionidaeNeodiprion L Kolomeits et al., 1972; Lyons, 1964
Pristiphora C Turnock, 1953Diprionidae
Diprion C Coppel et aI., 1974Neodiprion C Lyons, 1964;Pschorn-Walcher, 1965
Dermestidae CimbicidaePseudoclauellari C Benson, 1950
Coccinelidae PamphiliidaeNeurotoma L Benson, 1950
DiprionidaeNeodiprion L Lyons, 1964
Nematus A Benson, 1950Diptera
Asilidae TenthredinidaeTenthredo A Benson, 1950
DiprionidaeDiprion A Coppel et al., 1974
Monophadnus A Hobby, 1931aPteronidea A Hobby, 1931aSlrongylogaster A Hobby, 1931aAnthalia A Hobby, 1931aTenthredo A Hobby. 1932
266 Sylvio G. Codella, Jr. and Kenneth F. Raffa
TABLE IO.I (Continued)
Predator Prey StageO Representative references
Smirnoff, 1959Coppel and Benjamin, 1965
Adlung. 1966Benson, 1950
Carne, 1969Carne, 1961
TenthredinidaePristiphora LAmauronematu LPacynematus L
A, adult; C, coccon; E, egg; L, larva.
Bruns. 1954a,b: Adlung, 1966Benson. 1950Adlung, 1966
Adlung, 1966; Gosswald. 1941Coppel et al., 1974Adlung, 1966; Bruns, 1954a; IInitzsky.
1967; IInitzsky and McLeod, 1965;Knerer and Wilkinson, 1990;Kolomeits et at., 1972; Lyons, 1964;Morris et al., 1963; Schedl. 1938;Smirnoff, 1959
IInitzsky. 1967; IInitzsky and Mcleod.1965
Burke, 1932; IInitzsky, 1967; IInitzskyand Mcleod, 1965
probably also at risk due to the prolonged oviposition behavior of manyspecies (e.g., Ghent 1959), and we have observed them being transportedalong ant foraging trails. Ants have long been considered major selectiveagents for arthropod defense characters (Eisner, 1970; Pasteels et 01., 1983;Selman, 1988). This is largely due to their ubiquitous distribution, largenumbers, and social mechanisms of prey location, acquisition, and trans-port (reviewed by Traniello, 1989). Surprisingly, there has been little focuson the effects of prey defense on food selection and worker recruitment inants. Rather, most studies have evaluated the economics of food acquisitionin terms of prey item size (Traniello, 1983, 1987;Adarns and Traniello, 1981),quality (Crawford and Rissing, 1983; Sudd and Sudd, 1985), density (Be-rnstein, 1975), or predictability (Cosens and Toussaint, 1985, 1986). Antpredation in relation to arthropod defensive strategies therefore merits
10 Defense trategies of Folivorous awfties 267
increased attention, because such interactions are pervasive but poorlyunderstood.
Interestingly, some flower-visiting tenthredinids (e.g., Tenthredo spp.)supplement a pollen and nectar diet by preying on arthropods, includingother sawflies (Hobby, 1931a, 1932; Gauld and Bolton, 1988).
Vertebrate predators likely played an important role in the extinction amiearly diversification on various arthropod lines (Downes, 1987). However,their impact on present-day fauna is variable. Forest entomologists havelong recognized the importance of small mammal predation on diprionidcocoons and its influence on population behavior (Graham, 1928; Buckner,1955; Holling, 1959; Hanski and Parviainen, 1985). Shrews (Sorex spp.) andvoles (C/ethrionomys spp.) eat enormous numbers of cocoons and fre-quently hoard them for later consumption during the winter. Thus, thepredation period is effectively extended beyond the summer and autumnmonths (Buckner, 1967). Several authors (Hanski 1987; Olofsson, 1987)have argued that cocoon predation is a major factor in the populationdynamics of certain outbreak sawfly species.
Birds prey on all sawfly life stages, including the egg (Carne, 1969;Olofsson, 1986), larva (Buckner and Turnock, 1965; Atlegrim, 1989), cocoon(Coppel and Sloan, 1970; Coppel et 01., 1974), and adult (Buckner andTurnock, 1965; Carne, 1969). However, the actual effect of avian predationon sawfly population dynamics is unclear. In some habitats (e.g., tamarack[Larix /aricina] bogs; Buckner and Turnock, 1965), most avian species feedon sawflies, but in other cases such predation has been viewed as insignifi-cant (Benjamin, 1955; Kapler and Benjamin, 1960). Avian predation may beparticularly important at low prey population densities (Buckner, 1967;Atlegrim, 1989). Birds may also affect sawfly populations indirectly throughdispersal of pathogens (Entwistle et 0/., 1977a,b). Given the historical im-portance of birds in antipredator studies, increased attention in this area iswarranted. Holmes (1990) presents a particularly lucid overview of theecological and evolutionary effects of avian predation in forested eco-systems.
To summarize, the literature provides abundant evidence that sawfliesinteract with a variety of arthropod, mammalian, and avian predators,although the nature of these interactions (life stages, predators) is highlyvariable. Interestingly, most described sawfly defenses are evident in thelarvae, the stage for which the greatest variety of predators has beendescribed (Table 10.1) and for which predation is thought to playa minorrole in population regulation (Morris et 0/., 1963; Carne, 1969; Olofsson,1987). This suggests strong selection for antipredator characters at thisstage in the life cycle.
268 Sylvia G. Codella, Jr. and Kenneth F. RaIla
III. Escape in Time and Space
Endler (1986) identifies five stages in a successful predation event: detec-tion, identification, approach, subjugation, and consumption. At each stage,prey may counter predator efforts with a variety of defenses. At the detec-tion stage, prey can avoid certain natural enemies through asynchrony inactivity periods (Evans, 1990; an increase in "apparent rarity," Endler, 1986).Most conifer sawflies (Diprionidae) display a facultatively multivoltine lifecycle involving an overwintering, cocooned, prepupal stage (Coppel andBenjamin, 1965; Drooz, 1985). Adults of these species generally emerge inearly summer in northern latitudes, and their eggs are subjected to consid-erable pressure from parasites such as Closterocerus cinctipennis (Coppeland Benjamin, 1965). In contrast, several Neodiprion species display aunivoltine life cycle. Eggs are deposited in the autumn and hatch in earlyspring; thus, these insects avoid attack by many egg and prepupal parasites(Warren and Coyne, 1958; Kapler and Benjamin, 1960; Morris et al., 1963;Pschorn-Walcher, 1965; Betts, 1986; but see 010fsson,1987, for exceptions).Parasite avoidance is particularly evident in Neodiprion protti populationsin west Florida. Oviposition occurs during the cool period of late Novemberand early December, and eggs hatch by February, when parasite popula-tions are virtually nil (Knerer and Wilkinson, 1990).
In addition to facilitating parasite avoidance, a univoltine life cycle mayalso reduce exposure to cocoon predators under certain conditions. Innorthern Europe, cocoons of Neodiprion sertifer are in the soil for about 1month during the summer. In contrast, sympatric multivoltine speciesspend about 10 months overwintering in the cocoon stage. It has beensuggested (Hanski and Otronen, 1985; Hanski, 1987) that N. sertifer avoidsmuch predation pressure from small mammals and that this is a majorfactor in its outbreak behavior.
Sawflies can also spatially escape from predators. Some diprionids (e.g.,Diprion similis) spin cocoons directly on the foliage, as opposed to the soil,and thus appear to avoid contact with mammalian predators altogether,although this may increase exposure to insectivorous birds (Coppel andSloan, 1970; see also Hanski and Parviainen, 1985). Species that feed in thecrowns of mature trees probably reduce contact with many predators, suchas spiders and hemipterans. Ants may be an exception here, because manyforest species forage high in the canopy (Jeanne, 1979; Post and Jeanne,1982). The endophytic (Le., within-plant) oviposition behavior of manysawflies appears ancestral and may have provided a relatively benign devel-opmental environment in the past (Zeh et al., 1989). This characteristic mayalso assist in predator avoidance, because ants have been observed to crawlover tenthredinid (Heads and Lawton, 1985) and diprionid (S. G. Codella,personal observations) egg scars without notice. Constructed refugia alsospatially separate predator and prey, such as the communal, frass-filled
10 Defense trategies of Folivorous Sawflies 269
webs (Benson, 1950; Drooz, 1985) and leaf rolls (Drooz, 1985) of variouspamphiliids. The willow-feeding tenthredinid Stauronematus compressi-cornis, or palisade sawfly, constructs a barrier of dried saliva around itself(Boeve and Pasteels, 1985; Gauld and Bolton, 1988).
Sawflies may also avoid predators in the approach phase (Endler, 1986)through simple physical manuevers. Heads and Lawton (1985) reported thatthe bracken-feeding Tenthredo ferruginea drops from the frond when at-tacked by ants. Similarly, late-instar Neodiprion fuiviceps larvae drop frompine foliage when disturbed (Wagner et ai., 1986). While such behaviorprovides immediate antipredator benefits, it also incurs risks. Migration tonew host trees during the larval stage, such as during outbreaks or afterdislodgement by wind or rain, is highly hazardous (Benjamin, 1955; Ives,1963; Teras, 1982). Some small tenthredinid and argid adults also drop whendisturbed and then remain immobilized on the ground (Benson, 1950).
IV. Physical Defenses
Physical or mechanical defenses can interrupt the subjugation stage (End-ler, 1986) of the predation sequence. A number of tenthredinid larvae haveevolved a variety of protuberances or exuded coatings that appear tofunction in an antipredator context (Benson, 1950). For example, the hairsof the bracken-feedingStromboceros deiicatuius (Tenthredinidae) deter antpredation (Heads and Lawton, 1985). Among the British fauna, such struc-tures are markedly reduced among internal plant feeders (Benson, 1950),which further suggests a defensive function.
The Rosaceae-feeding pear slug, Caiiroa cerasii (Tenthredinidae: Heter-arthrinae), secretes a slime layer that presumably deters both invertebrateand vertebrate predators (Fig. 10.1; Benson, 1950; D. R. Smith, 1971). Certaineriocanine and allantinine tenthredinid larvae exude waxy coverings fromcuticular glands (Dusham, 1928; Percy et ai., 1983). Among adults, the largertenthredinids (e.g., Tenthredo spp.) bear large mandibles that can inflict apainful bite (Benson, 1950).
V. Chemical Defenses
About half of the arthropod orders include species with chemical defenses(Whitman et ai., 1990), and over 600 such compounds have been identified(Blum, 1981). Among the sawflies, it is these responses to the subjugationphase (Endler, 1986) that have been the most elaborated over evolutionarytime. Table 10.2 summarizes putative chemical defenses in the Symphyta.
270 Sylvio G. Codella, Jr. and Kenneth F. Raffa
FIGURE 10.1 Larva of the slime-secreting pear slug, Caliroa cerasii (Tenthredinidae: Heter-arthrinae).
All known cases are solely manifested in the larval stage, with residualdefenses persisting into the cocoon period of regurgitating dipironids andpergines. The defenses appear quite variable with regard to such factors asallomone composition and origins (Fig. 10.2), methods of storage and re-lease, and the range of efficacy.
A. Modes of Storage and Delivery
Most symphytan chemical defenses involve discrete (i.e., localized) storageof allomones (Table 10.2). In diprionids and in some pergids (Perginae),allomones are sequestered in foregut outpocketings. Diprionid larvae pos-sess a pair of esophageal diverticulae, which is a unique derived characterof the family (Fig. 10.3; Maxwell, 1955). The resinous contents, which areobtained from the host plant (Pinaceae; see section V.B), are regurgitated inresponse to harassment (Fig. 10.4; Britton and Zappe, 1918; Benson, 1950).This behavior has been shown to repel ants, pentatomid bugs, spiders, andbirds, as well as hymenopteran and dipteran parasites (Prop, 1960; Tripp,1960; Tostowaryk, 1972; Eisner et al., 1974). Being foregut components, thediverticulae are cuticle-lined, but the contents are retained during larvalmolts by the fragmentation of the lining (Eisner et at., 1974). The material isfinally lost during prepupal ecdysis within the cocoon; a granular plug formsat the posterior base of the stomodeum, and the structure is shed intactwith the exuvia (Phillipsen and Coppel, 1973). Larvae thus retain theirdefensive capabilities within the cocoon until pupation (Eisner et al., 1974).
A similar system is present in some pergids (Perginae); however, mor-phological differences suggest that the structures are not homologous withthose of diprionids (Maxwell, 1955). In this instance, a voluminous bilobeddiverticulum fills the ventral thoracic area. It originates anterior to thediprionid pouches, entering the pharynx near the mouth (Maxwell, 1955). As
10 Defense Strategies of Folivorous Sawflies 271
TABLE 10.2 Sawfly Chemical Defenses
Taxon StageQ Mode Site Originb References
Megaxyela L Eversible Cervical ? Yuasa, 1923;glands Maxwell,1955
PergidaePerginae L,C Regurgitation Pharyngeal H Carne, 1961;
Morrow et 01.,1976
PterygophorinaeLophyrotoma L Systemic ? A? Williams et 01.,
ArgidaeArginae L Reservoir Ventral- ? Maxwell,1955
glands abdominalAtomacerinae L Reservoir Ventral- ? Maxwell,1955
glands abdominalSterictophoinae L Reservoir Ventral- Maxwell,1955
glands abdominalSericocerinae L Reservoir Ventral- Maxwell, 1955
glands abdominalCimbicidae L Reservoir Spiracular H? Benson, 1950;
Diprionidae L,C Regurgitation Esophageal H Prop, 1960;Eisner et 01.,1974
Strongylogaster L Systemic Hemolymph Heads andLawton, 1985
Aneugmenus L Systemic Hemolymph ? Heads andLawton, 1985;Heads, 1986
Nematinae L Eversible Ventral- A,H? Boeve et 01.,glands abdominal 1984; Jonsson
et 01., 1988Heterarthrinae
Caliraa L Eversible Prothoracic Yuasa, 1923glands
AllantinaeAmetaslegia L Systemic? H? Bowers, 1980
TenthredininaeTenlhredo L Systemic? H Bowers, 1990
U C, cocoon; L, larva.b A, autogenous; H, host plant.
272 Sylvio G. Codella, Jr. and Kenneth F. Raffa
PhCO-o - Ala -0- Phe-L-Val-L-lIe- O-Asp-L-Asp- o-Glu - L-Gln
cis, trans - Dolichodial
FIGURE 10.2 Representative chemical defenses in the ymphyta. (A) a-Pinene, a monoter-pene. (B) Abietic acid, a diterpene resin acid. Both (A) and (B) are common in diprionid larvalregurgitation. (C) Lophyrotomin, an octapeptide with four D-arnino acids found in Lophy-rotoma inteffupta larvae (Pergidae: Pterygophorinae). (D) Benzaldehyde, a common com-ponent of nematine (Tenthredinidae) eversible gland secretions. (E) cis,trans-dolichidial, thesole compound of Croseus varus, another nematine with eversible glands.
with diprionids, pergine larvae regurgitate a host-based (Eucalyptus) vis-cous fluid when disturbed and thus deter invertebrate and vertebrate preda-tors (Evans, 1934; Carne, 1962; Morrow et aI., 1976). Diverticular contentsare incorporated into the cocoon wall in this case (Carne, 1962).
Regurgitation in these sawfly taxa is notable in that specialized struc-tures house the orally released allomones. Myrascia caterpillars (Lepidop-tera: Oecophoridae) possess a single foregut diverticulum and bear manyother similarities to the sawfly examples (Common and Bellas, 1977).However, while enteric discharge is a common arthropod defense strategy(table in Whitman et al., 1990), it more commonly involves the release offluids directly from the gut (Bowers, 1990). Common examples include"spitting" grasshoppers (Acrididae; Eisner, 1970; Blum, 1981) and the tentcaterpillars (Lasiocampidae: Malacosoma spp.; Peterson et al. 1987). Thecorrelates of diverticular sequestration have not yet been fully explored.Systemic allomone storage may often evolve initially as a means of over-coming host defenses (Brower et af., 1988), but whether or not localizedaccumulation of host allomones evolved under a similar scenario is un-clear.
10 Defense trategies of Folivorous Sawflies 273
FIGURE 10.3 Resin-filled foregut diverticulae (arrows) of eodiprion sertifer (Diprionidae).
FIGURE 10.4 eodiprion sertifer larvae displaying defensive posturing during regurgitation.
274 Sylvia G. Codella, Jr. and Kenneth F. Raffa
Eversible glands are another form of localized allomone storage. Theseinvaginated structures are associated with secretory glands and are evertedby hemostatic pressure (Whitman et 01., 1990). The osmeterium of papilio-nid caterpillars is a well-known example (Eisner and Meinwald, 1965;Honda, 1983). Tenthredinids of the subfamily Nematinae possess a series ofsuch structures on the medioventral surface of abdominal segments 1-7(yuasa, 1923; Maxwell, 1955). In Pristiphora spp., the glands on the firstsegment are noneverting (Jonsson et 01., 1988). The glandular secretionshave been shown to deter ants and birds effectively (Boeve and Pasteels,1985; Jonsson et 01., 1988). Boeve and Pasteels (1985) noted an associationbetween large glandular surface area and a high degree of unpalatability tobirds. Other tenthredinids and some xyelids have paired eversible glandsoriginating laterally in the cervical region (Yuasa, 1923; Maxwell, 1955), but,to our knowledge, the functional aspects of these remain unstudied.
The most common defensive glands in arthropods are noneversiblereservoirs, whose contents are expelled under pressure (Whitman et 01.,1990). Cimbicid larvae possess a paired series of such glands above thespiracles (Benson, 1950) and forcefully eject fluid when handled. The Ar-gidae displays an impressive variety of reservior glands among severalsubfamilies, but we are unaware of any studies on their function. Thesediverse structures include the so-called milk-bottle glands of the Atom-acerinae and Sterictiphorinae (Maxwell, 1955) as well as various abdominalglands in other subfamilies.
Systemic storage of allomones is also known in symphytans and may bemore widespread than present information indicates. The Australian"cattle-poisoning" sawfly, Lophyrotoma interrupta (Pergidae: Pterygopho-rinae), aggregates in large numbers at the base of its host tree, Eucalyptusmelanophloia, during outbreak years when foliage becomes scarce. Grazingcattle and sheep actively seek these masses and feed voraciously on them.The lifestock subsequently suffer seizures and liver necrosis, generallyresulting in death (Oelrichs, 1982; MacKenzie et 01., 1985). The chemistry ofthe situation is unusual (see Section V.B, below), but its ecological signifi-cance has not been studied. Various other tenthredinids possess sticky ordistasteful hemolymph (Table 10.2), which is repellent to ants (Heads andLawton, 1985), and Heads (1986) reported that certain Aneugmenus larvaeautohemorrhage this material upon harassment.
In many instances, these chemical defenses are preceded by or releasedconcurrently with physical posturing. Diprionid larvae often laterally sweepthe anterior half of the body rigorously before resorting to regurgitation andmay arch back in a "U-bend" when exuding resin (Prop, 1960). Similarly,nematine larvae expose their abdominal glands by rearing the abdomenquickly in a "snap-bend" posture (Jonsson et 01., 1988). Such multicom-ponent defensive repetoires (Pearson, 1989) can allow prey to respond to avariety of predators and increase a trait's efficacy by combining it withcomplementary characters.
10 Defense lrategies of folivorous awfties 275
B. Sources and Composition of Allomones
Sawfly defensive secretions are often complex mixtures with diversechemical structures and properties (Fig. 10.2). While many of these havebeen chemically characterized, their origin (host-derived, autogenous, orboth) and range of efficacy remain poorly understood.
Diprionids fill their diverticulae with host compounds in an apparentlyunselective manner. Larvae feed on foliage of Pinaceae and thus acquirevarious terpenoids (Eisner et al., 1974), including mono- and sequiterpenesand diterpene resin acids (Fig. 10.2). The volatile components are highlyrepellent, particularly to arthropods (Eisner et al., 1974), and are toxic athigh concentrations (e.g., a-pinene in papilionid osmeterial secretions;Honda, 1983). The nonvolatile resin component of regurgitation hardensafter contact, thus entangling arthropod predators, and also retards theevaporation of the volatile monoterpenes (Eisner et al., 1974). Larval terpe-noid profiles are essentially identical to those of the host diets (Eisner et al.,1974) and vary with host species and individual (Codella and Raffa, unpub-lished data). Thus, there is no evidence of selective sequestration of partic-ular host components, as is known in some other systems (e.g., the nympha-lid butterfly Euphydryas phaeton on Plantago lanoceatata; Bowers, 1988).Likewise, early- and late-instar larvae reared on identical diets do not differin relative terpenoid composition (Codella and Raffa, unpublished data).
The pergine regurgitation system is similar in many respects. Eucalyp-tus essential oils are sequestered unaltered in the diverticulum (Carne,1962; Morrow et aI., 1976). The major component found by Morrow et al.(1976) in Eucalyptus pauciflora was a mixture of eudesmol isomers. OtherEucalyptus species contain larger amounts of mono- and sesquiterpenesand volatile aldehydes (Morrow et al., 1976). As with diprionids on pines,larval exudates vary with host diet (Morrow et al., 1976). Among otherPergidae, the toxic peptide in Lophyrotoma, called lophyrotomin, containsfour Damino acids and, as SUCh, appears unique among animals (Fig. 10.2;Williams et al., 1982); however, whether the material is synthesized de novoor sequestered from external sources is not clear.
The spiracular glands of cimbicids may also contain host derivatives.Sevastopulo (1958) noted that the ejected fluid of aSalix-feeding species inAustria had a bitter taste similar to that of its host leaves.
The abdominal secretions of nematines are particularly variable andoften complex mixtures. To date, 18 compounds have been isolated fromthe exudates of 11 woody-plant-feeding species in the genera Nematus,Nematinus, Croesus, Pontania, and Pristiphora (Boeve et al., 1984; Jonssonet al., 1988; Duffield et al., 1990). These taxa are broadly similar in that theirsecretions contain various volatiles such as benzaldehyde, oxygenatedmonoterpenes, and acetates (Fig. 10.2), but the mixtures show considerableinterspecific variation. For example, Croesus varus secretes a single com-pound, cis,trans-dolichodial (Fig. 10.2), while eight components have been
276 Sylvio G. Codella, Jr. and Kenneth F. Ralfa
isolated from Pristiphora erichsonii. Jonsson et al. (1988) fed P. erichsoniiand Pristiphora wesmaeli identical Larix diets but found considerable quali-tative and quantitative differences in their secretions. They noted, however,that the oxygenated monoterpenes present may be derived from host terpe-noids, as is the case in some bark beetles (Coleoptera: Scolytidae). Theorigin of nematine allomones is therefore still unclear.
Two patterns emerge from this survey. First, known sawfly chemicaldefenses, both putative and demonstrated, are limited to the larval stage.Diprionid adults and eggs, for example, do not contain measurable quanti-ties of the compounds found in larval regurgitation (Codella and Raffa,unpublished data). Second, most sawfly allomones are discretely ratherthan systemically stored and act as physical deterrents or general irritants,which appear to be most effective against invertebrates (Pasteels et al.,1983). Taken together, these points suggest that most symphytan defenses,to the extent that they are adaptations in the strict sense, evolved as larvaldefenses against invertebrate natural enemies. While Prop (1960) noted thatdiprionids can effectively place regurgitant droplets in response to avianharassment, localized, ejectable defenses seem most suited against preda-tors (and parasites) on the same-size scale (Pasteels et al., 1983). Anotherpossibility is that diprionid and pergine diverticulae evolved in anothercontext and, as such, were preadaptations (or exaptations; Gould and Vrba,1982) for defense (see Section VIII).
C. Development and Behavior in Relation to Chemical Defense
The concept of a metabolic cost being associated with sequestration of hostcompounds for defense has been a recurrent one (Brower et at., 1972;Brower and Moffit, 1974; Cohen, 1985; Bowers, 1989). Brower et al. (1972)suggested that by sequestering cardenolides from Asceplias host plants,monarch butterflies, Danaus plexippus (Danaidae), might suffer substantialreductions in such parameters as weight or fecundity. Several subsequentstudies involving monarchs or other organisms failed to find evidence ofallomone-associated cost (Erickson, 1973; Isman, 1977; D. A. S. Smith, 1978)or achieved variable results (Brower and Moffitt, 1974). Such findings,however, may be due to the confounding effects of sex and geographiclocation (Cohen, 1985). It is clear that the notion of cost-bearing defenses isa complex one that will not be soon resolved (Bowers, 1989).
The diprionid sawflies provide an interesting perspective on this con-troversy. Regurgitation of enteric contents may be a relatively low-costdefense strategy (Blum, 1981). Diprionid larvae possess cuticle-lined diver-ticulae and do not modify incoming host compounds and, thus, fit thisgeneralization. However, the situation is again complex. Larsson et al.(1986) reared N. sertifer on low (1.5%) and high (5.2%) terpenoid clones ofScots pine, Pinus sylvestris. The high-terpenoid clone increased develop-
10 Defense Strategies of Folivorous Sawflies 277
ment time and decreased survival, but relative growth and consumptionrates actually increased. Furthermore, larvae on the low-terpenoid clonefed more frequently on bark and on the basal area of needles, both of whichare higher in resin acids, than larvae reared on the high-terpenoid.clone.lna subsequent study (Bjorkman and Larsson, 1991), larvae on the high-terpenoid clone were harassed with foreceps and their exudates collected.These insects fed more extensively on bark and needle bases (Le., high-terpenoid tissues) and, in contrast to the earlier study, showed reducedconsumption and growth rates. Larvae reared on the high-terpenoid clonewere also better-defended against ant predation in field experiments.
The cost of terpenoid-based defense in conifer sawflies may also bereflected in other parameters. Neodiprion sertifer larvae reared on jack pine,Pinus banksiana, produce more regurgitation and are better defendedagainst wood ants than those reared on red pine, Pinus resinosa; however,females reared on P. banksiana have lower cocoon weights (Codella andRaffa, 1990 and unpublished). Cocoon weight is well correlated with fecun-dity in diprionids (Popo, 1968; Codella et al., 1991); thus, a single dietappears to both increase the probability of survival and decrease reproduc-tive success. These results vary with the host range; the relatively polypha-gous Neodiprion lecontei, which can complete the larval period on at leastfive coniferous genera (Benjamin, 1955; Benjamin and All, 1972), does notexhibit the same conflict between development and defense seen in themore host-restricted N. sertifer. In both cases, larvae strongly prefer P.banksiana in feeding choice assays.
Heliovaara et al. (1990) provide an interesting perspective on thissituation. Using all-male clutches from unmated females, they demon-strated that while smaller females are less fecund, a greater proportion oftheir eggs are viable compared to larger females. The number of hatchingsis thus fairly independent of female size. How these results relate to morenatural conditions is not clear, because diprionid sex ratios are generallyfemale-biased (Schedl, 1939; Lyons, 1964; Henson et al., 1970), and malessuffer greater mortality than females in the egg and early larval stages(Lyons and Sullivan, 1974). In any event, sawflies may continue to yieldintriguing data regarding the cost of chemical defense.
VI. Camouflage, Aposematism, and Mimicry
In the broad sense, protective coloration can function during both thedetection (camouflage) and identification (aposematism and mimicry)stages of predation (Endler, 1986). These strategies are not restricted to thevisual modality (Pasteur, 1982; Evans and Schmidt, 1990), but historicalemphasis limits consideration here. Despite a literature rife with intriguing
278 ylvio G. Codella, Jr. and Kenneth F. RaIla
anecdotes, in no instance has the efficacy of putative aposematic colorationactually been demonstrated in the Symphyta. Prop (1960) offered trays of nvarious larvae to both wild and caged birds and showed that certain pat- sterns were more conspicuous than others in that context; however, he did Enot document that particular color schemes reduced learning time in indi- avidual predators in a suitably controlled environment (e.g., Codella and (Lederhouse, 1990) or explore other possible mechanisms (Guilford, 1990). tMany subsequent studies assumed the defensive utility of various sawfly ~patterns as a starting point (Boeve and Pasteels, 1985; Sillen-Tullberg,1990). Thus, intensive study of sawfly coloration is needed before general-izations are possible.
Larval Symphyta display a wide variety of coloration (e.g., see plates inRose and Lindquist, 1980, 1982, 1984, 1985). Various patterns in Diprionidaeand Perginae have long been interpreted as either aposematic or cryptic(Benson, 1950; Prop, 1960; Carne, 1962). In nematine larvae, the degree ofconspicuousness, which is highly variable, is loosely correlated with eversi-ble gland surface area (Boeve and Pasteels, 1985). Many Tenthredo adultsresemble bees or wasps (Hobby, 1931b; Benson, 1950) and provide a possi-ble example of Batesian mimicry in the Symphyta. The bold coloration ofthe larvae of many chemically defended diprionid species is broadly similar,which suggests Mullerian convergence (Gilbert, 1983).
Coloration must be viewed from a more dynamic, multifunctional per-spective if we are to place antipredator strategies in the appropriate context(Moynihan, 1981; Endler, 1990). To evaluate these observations, three keyfactors must be considered. First, sawfly coloration must be evaluatedagainst the background(s) against which the sawfly rests. Diprionids spendthe larval stage against the green cast of conifer foliage (unlike the manyinsects whose background constantly changes). Prop (1960) recognizedthis and performed his feeding trials with a green tray. Disruptive patterns,which blend the organism's outline into the general environment (a form ofeucrypsis; Pasteur, 1982), require a mixed rather than a uniform back-ground (Cott, 1940; Edmunds, 1990). Thus, the mottled pattern of the intro-duced pine sawfly, D. similis, which is often considered disruptive (Coppelet al., 1974), may not actually function in this context. The redheaded pinesawfly, N. lecontei, is bright yellow, and late-instar individuals possessseveral rows of black spots. To human observers, colonies of this sawfly arequite conspicuous at close range but are often lost in the glare of the sunwhen observed at a distance (Codella personal observations). The effect ofsuch crypsis may potentially be countered by larval foliar damage, whichcan be used as a search image by avian predators (Heinrich and Collins,1983). Thus, the pattern ofN. lecontei (and that of similarly colored sawflies)may be both a primary and secondary defense mechanism (Lederhouse,1990) and provide protection in two different contexts. Background in thebroad sense, including prevailing environmental conditions, must be con-sidered in a holistic study of defensive coloration.
10 Defense Strategies of Folivorous awllies 279
Second, the behavioral and sensory capacities of the relevant predatorsmust be considered. We suggested earlier (see Section II.B) that manysawfly chemical defenses evolved in response to invertebrate predation.Because of their chemically based sensory systems, invertebrate predatorsare not considered major selective agents in the evolution of aposematism(Pasteels et al., 1983; but see Berenbaum and Miliczky, 1984). Among verte-brates, only birds seem to interact with larvae to any great degree (seeSection II.B); therefore, we must evaluate sawfly color patterns from anavian perspective. Despite the widespread assumption that humans andbirds see the world in the same way (Prop, 1960), ample evidence indicatesthat this is not so (references in Endler, 1990). Endler (1990) warns of thepitfalls of such a subjective approach to the evaluation of defensivecoloration and discusses methods of objectively measuring animal andbackground patterns from the perspective of the receiver. Initial humanperceptions are a necessary starting point that must ultimately give way tomore objective evaluation.
Finally, researchers must recognize the constraints imposed on patternevolution by other needs. Coloration may reflect compromises betweenconflicting selection pressures (Endler, 1978) involving, for example, ther-moregulation or mate recognition (Cott, 1940; Edmunds, 1974; Endler, 1978;Guilford, 1990). Many univoltine Neodiprion species, whose overwinteringeggs hatch in early spring, have darkly colored larvae. Such colorationconceivably has thermoregulatory advantages, because larvae are oftenexposed to near-freezing temperatures in northern climates. The patternsmay still be aposematic (Sillen-Tullberg, 1990) and, thus, function in twodifferent contexts. To date, however, neither utility has been demonstrated.
VII. Gregarious Behavior: Multiple Selection Pressures?
Group living can confer a variety of physiological, reproductive, and defen-sive benefits, but it also potentially carries competitive and predatory costs(Bertram, 1978; Rubinstein, 1978; Vulinec, 1990). Gregariousness is wide-spread in the Symphyta, with representative species in the Pamphiliidae,Argidae, Pergidae, Diprionidae, and Tenthredinidae (Evans, 1934; Benson,1950; Atwood, 1962; Eickwort, 1981; Boeve and Pasteels, 1985; Drooz, 1985;Boeve, 1991). Such behavior has been explained in terms of development(Ghent, 1960; Henson, 1965), predation (Fisher, 1930), and parental care(Dias, 1982). In the Diprionidae, the likelihood of gregariousness is probablyaffected by many factors (Fig. 10.5), the influence of which likely varies withpopulation density. The family exhibits a broad range of group sizes, whichpartly results from variation in egg clustering by ovipositing females (Fig.10.5; Atwood, 1962). The issue, however, is clearly complex, and a completeexplanation requires consideration of many life history characters.
280 Sylvio G. Codella, Jr. and Kenneth F. Raffa
EGG PREDATORCLUSTERING BEHAVIOR
~;V1V~ j~VELQPt.IENTPREDATION "Yo;;;
y +1 1~CONSPICUOUSNESS + DILUTIONDEFENSESIGNAlS
fiGURE 10.5 Potential influences and consequences of gregarious behavior in diprionidlarvae.
A. DiseaseA major disadvantage to larval gregariousness is the high potential fortransmission of nuclear polyhedrosis virus (NPV; Cunningham and Ent-wistle, 1981). Crowding has been implicated in insect epizootics in general(Steinhaus, 1958), and viral transmission in gregarious diprionids is density-dependent (Bird, 1953). The majority of sawflies with known viral associa-tions are in the Diprionidae (Cunningham and Entwistle, 1981), and thepathogens are considered by some to be an important factor in sawflypopulation regulation (Coppel and Mertins, 1977, but see Olofsson, 1987).Within aggregations, NPV can be transmitted through frass, cadavers, anddefensive regurgitation (Cunnigham and Entwistle, 1981; Entwistle et al.,1983), and infection rate increases wi th aggregation size at certain tempera-
10 Defense Strategies of Folivorous awOies 281
tures (Fig. 10.5; Mohamed et at., 1985). Transmission between aggregationsis related to colony distance and density (Young and Yearian, 1990).
Various developmental advantages to group living have been demonstratedin insects. Larval development may accelerate as the result of increasedfeeding and growth rates (McFarlane, 1962; Lockwood and Story, 1986;Ribeiro, 1989; Lawrence, 1990; Stamp and Bowers, 1990b), increased wateruptake (Lockwood and Story, 1986), or improved thermoregulatory options(May, 1979; Stamps and Bowers, 1990a). Survivorship may also increase dueto improved feeding efficiency (Ribeiro, 1989; Lawrence, 1990) or the re-duced probability of cannibalism (Breden and Wade, 1987).
Aggregation increases early-instar survival in some diprionids (Fig.10.5; Ghent, 1960; Nakamura, 1981; see also Carne, 1969, for pergids).For example, first-instar larval mortality in Neodiprion pratti banksianaereaches 80% in solitary laboratory rearings but drops to about 50% forgroups of four (Ghent, 1960). This may result from variation in individualability to initiate feeding incisions in the tough pine needle cuticle, becausesolitary larvae placed on artificial wounds feed readily (Ghent, 1960). Thus,aggregation may increase the probability that some members of the groupcan initiate a feeding site that other larvae can exploit.
However, social facilitation of feeding does not fully explain diprionidgregarious behavior. Other studies have shown conflicting results. In con-trast to Ghent's findings, N. pratti survival did not vary with group size in astudy by Kalin and Knerer (1977), although development time did (Fig. 10.5).Neodiprion abietis mortality actually increased with larval density in thesame experiment. Neodiprion sertifer has also been reared successfully inisolation (Henson, 1965). Beyond this variability, however, are more generalconcerns. Diprionid larvae are capable of feeding independently within 5-7days of hatch (Ghent, 1960; Nakamura, 1980b). The potential costs of gregar-ious behavior might therefore be expected to favor colony splitting duringthe later larval stages (Fig. 10.5), as is seen in D. similis (Coppel et at., 1974),but most species remain aggregated. This strongly suggests that otherfactors are involved. There are other possible developmental advantages,but results are somewhat conflicting (Ghent, 1960; Henson, 1965; Kalin andKnerer, 1977). In general, colony size does not appear to affect survival ordevelopment time when averaged over the entire larval period (Ghent, 1960;Kalin and Knerer, 1977; Nakamura, 1980a,b). Other possible developmentalbenefits of aggregation merit further investigation in sawflies. In the perginePerga dorsalis, aggregation increases digestive rates, reduces convectiveheat loss, and improves the efficiency of heat loss behaviors (Seymour,1974). Thermoregulatory advantages of aggregation may be enhanced bydark coloration (see Section VI and Fig. 10.5). In Diprion pini, diapause
282 Sylvio G. Codella, Jr. and Kenneth F. RaIfa
incidence increases from about 30 to 48% in larger aggregations and mayexplain the increased diapause incidence seen near the conclusion of out-breaks of this species (Geri and Goussard, 1989). The developmental bene-fits of diprionid gregariousness, therefore, are still not fully understood.
Antipredator benefits to aggregated insect prey are well documented (Al-drich and Blum, 1978; Lawrence, 1990; Lockwood and Story, 1986; Ribeiro,1989; Terhune and Foster, 1982; Vulinec and Miller, 1989). In addition toreducing the per capita probability of predation (Hamilton, 1971), gregariousbehavior often provides other antipredator benefits or is accompanied byadditional lines of defense (Vulinec, 1990). Sawfly gregarious behavior haslong been interpreted as a defense adaptation (Fisher, 1930; Carpenter andFord, 1933; Cott, 1940). There probably are predatory disadvantages toaggregation at certain points in the life cycle, but these must be evaluatedfrom a total perspective. In Neodiprion swainei, for example, egg parasitismincreases with cluster size, but hatchling survival increases with colony size(Lyons, 1962; see also Nakamura, 1981). In many respects, the defensehypothesis is an attractive one. In many diprionid species, colony sizeusually far exceeds the number of larvae needed to satisfy Ghent's (1960)social facilitation hypothesis. Females of many species deposit their entireclutch (ca. 50-100 eggs) in a single shoot (Coppel and Benjamin, 1965).Several females may select the same shoot for oviposition (Codella andRaffa, unpublished data) and individual colonies may coalesce (Tosto-waryk, 1971b; see also Carne, 1962, on pergids). As a result of these factors,larval aggregations may contain several hundred individuals, which may attimes be composed of more than one species (Codella, personal observa-tions).
Additionally, gregariousness can be viewed at several levels of organi-zation. In contrast to broad-leaved trees, conifer needle architecture greatlyrestricts the number of individuals that can occupy a single foliar unit; thus,aggregations really consist of numerous subgroups. For example, late-instarNeodiprion nanulus nanulus average about eight larvae per needle withinan aggregation on P. resinosa (Codella and Raffa, unpublished data). Thesesubgroups can coordinate defensive responses. When larvae on one needleare disturbed, adjacent subgroups respond nearly 70% of the time (Codellaand Raffa, unpublished data). However, the spatial separation of the sub-groups probably limits the utility of this response, especially against smallarthropod predators. On a larger scale, females of the nematine Croesusseptentrionalis appear to aggregate for oviposition at particular trees withina stand, creating a large "superaggregation" of larvae (Boeve, 1991). Simi-larly, in young red pine (P. resinosa) stands (mean tree height 1.8 0.56 m).the probability of a tree being used as an oviposition substrate by N. lecontei
10 Defense trategies of Folivorous Sawflies 283
increases with its prior defoliation. In some cases, trees with over 75%needle loss receive over 1000 eggs (Codella and Raffa, unpublished data).Assuming a high hatch rate, this apparently maladaptive behavior virtuallyassures that larvae will have to migrate before development is completed.However, the antipredator benefits accrued (signal amplification?) maycounter this cost.
In our view, the potential defensive benefits of sawfly gregarious behav-ior fall under two general categories: amplification of signals and defenses,and dilution ("selfish herd"; Hamilton, 1971) effects, which lower individualrisk (Fig. 10.5). Conversely, aggregation may also increase conspicuousnessand therefore the probability of discovery by some predators (Fig. 10.5). Inthe case of amplification, we see at least three possibilities, all of which canpotentially be in operation. First, aggregation may magnify aposematiccoloration (Fig. 10.5). For example, the conspicuous C. septentrionalis formslarger aggregations than the cryptic C. varus (Boeve, 1991). Vulinec (1990)observed that this popular idea, which can be traced to Fisher (1930), hasnever actually been verified in any organism. Aposematism is not an essen-tial component of gregariousness (Hamilton 1971), and recent work sug-gested that the former often precedes the latter (Sillen-Tullberg, 1988).Diprionids, with their diversity of color patterns, group sizes, and behav-ioral thresholds (see following paragraph), provide an excellent opportu-nity to explore the hypothesis in detail.
A second possibility for signal amplification involves warning behaviorsenhanced by synchronous performance. There is already some evidence forthis in the Diprionidae. Prop (1960) found that larval jerking behavior priorto regurgitation induced startle responses in captive birds, which generallyabandoned the larvae afterward. Although the data set is not large, there issome indication that larger groups elicited a greater response. He also notedinterspecific differences in the degree of sawfly response. More recently,Sillen-Tullberg (1990) demonstrated that aggregated (n = 20) N. sertifersuffer fewer attacks from great tits than solitary individuals. She attributedthis to the synchronized behaviors seen in larval aggregations.
Finally, gregariousness may directly increase defensive efficacy (Vul-inec, 1990). As already noted, many sawflies are remarkably synchronized intheir regurgitation behavior, and this results in a large volume of deliveredallomone. Much of this material is spread on adjacent sawflies duringdefense (Eisner et al., 1974), which may provide some residual protection.As diprionid group size increases beyond 20 larvae, Podisus modestus(Hemiptera: Pentatomidae) predatory success declines due to increasedprey handling time, which results from greater defensive efficiency(Tostowaryk, 1972).
Dilution effects may also be in operation and can be modified behav-iorally. Within smaller aggregations, N. lecontei larvae continually shiftposition on both the foliage and adjacent neighbors. As a result, no individ-
284 Sylvio G. Codella, Jr. and Kenneth F. Raffa
ual remains in an exposed position for long (Codella and Raffa, unpub-lished). Tostotowaryk (1971b) found that diprionid larvae at the peripheryof large groups were more likely to be parasitized that those at the interior.This emphasizes the dilution benefits of group living but also suggests thatoptions for movement are reduced in larger colonies.
AIthough ants retrieve more N. sertifer larvae from large (n = 40) versussmall (n = 5) aggregations in field experiments, individual risk of predationis significantly less in large groups (Codella and Raffa, unpublished data).Dilution may also be in effect over the long term due to behavioral desensi-tization. For example, ants may become acclimated to larval presence atfrequently visited areas, such as near aphid aggregations. In a naturalsituation, we observed Formica obscuripes workers lifting second-instarNeodiprion maurus larvae in their mandibles only to place them on thesubstrate again in the absence of any obvious defensive behavior. Early-instar diprionids show relatively low defensive potential against ants andare thus highly vulnerable to predation (Codella and Raffa, unpublisheddata). Such observations emphasize the importance of evaluating long-terminteractions between predators and prey.
These hypotheses are not mutually exclusive. The factors influencinggroup living, as well as the advantages gained, may vary over the larvalperiod, and several may operate simultaneously (Fig. 10.5). More detailedstudy of sawfly gregarious behavior is needed.
VIII. Conclusions and Prospects
In this chapter, our goal was to provide a broad overview of defense in theSymphyta. We identified several areas, particularly coloration and gregari-ousness, where further work is particularly needed. New studies will un-doubtedly yield exciting information, and the results should prove valuableto many branches of biology.
Rarely have many differing aspects of an insect's defensive biology beenaddressed within a single system (Bowers, 1990). Likewise, the ontogeny ofdefense strategies (chemistry, coloration, behavior) throughout the lifehistory of organisms requires further attention (Cornell et al., 1987). Thediverse life-styles and defenses of sawflies provide an ideal opportunity forsuch an approach. This need of integration can be illustrated by recallingsome previously discussed aspects of N. sertifer biology. Many early-seasondiprionids are darkJy hued, and this conceivably could be related to thermo-regulation (see Section VI). This does not, however, rule out aposematism insuch species, even if coloration per se is not involved. Prop (1960), followingCott (1940), emphasized the need to view conspicuousness as a suite oftraits. Neodiprion sertifer, a dark spring species, is highly aggregated and
10 Defense Strategies of Folivorous Sawflies 285
among the most reactive of diprionids to visual stimuli (Prop, 1960). In thiscase, aggregation and synchronized displays are perhaps the true apose-matic signal. Interestingly, N. lecontei, which is conspicuously colored withyellow, red, and black, is far less concerted in its behavioral displays. Thus,the true role of putative sawfly defenses may at times be obscured when thecharacters are viewed in isolation.
In our view, a major area requiring further work is the evolution ofdefensive regurgitation. Several factors suggest that diverticular storageinitially evolved as a means of overcoming host plant defenses and subse-quently played a role against natural enemies (Eisner et al., 1974; Morrow etal., 1976; Common and Bellas, 1977). In the Diprionidae, all species bothpossess esophogeal pouches (see Section VA) and feed on conifer foliage.We predict that detoxifying enzyme activity should be low in diprionids(particularly in the foregut region) versus other taxa that lack diverticulaeyet utilize the same hosts. To date, little work has been done on symphytandetoxification systems (Kreiger et al., 1970; Rose, 1987); however, Rose's(1987) work offers some intriguing suggestions. The Eucalyptus-feedingpergine Pergagrapta polita possesses foregut diverticulae. While enzymeactivity is high in the anterior midgut, it is quite low in the foregut. Thisshould facilitate sequestration of allomones in an unaltered state, whereasmaterial not so stored can be detoxified in the midgut. Comparisons toEucalyptus-feeding pergids in other (diverticulae-Iacking) subfamilies (e.g.,Pterygophorinae) would be valuable here.
A second reason for suspecting a host utilization origin of diverticulaeis that such storage appears to have been relatively unmodified over time.Sequestration is nonselective, does not vary with instar, and is not carriedover to other life stages. This may reflect a compromise between hostutilization and defense functions. It is likely that such a trait was initiallyused against generalist arthropod predators (e.g., non-web-buildingspiders, ants) that were already present on conifers.
We thank Greg LintereuI for his photographs. Some of our work described here wassupported by the USDA Mcintire-Stennis Program and by the University of Wisconsin-MadisonCollege of Agriculture and Life Sciences.
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