Table Of ContentVol. 3No.1 1996 SCRIBER: Antheraea Larval Growth 23
HOLARCTIC LEPIDOPTERA, 3(1): 23-30
NOTES ON LARVAL GROWTH
AND EFFICIENCIES IN ANTHERAEA:
A. POLYPHEMUS AND A. PERNYI
(LEPIDOPTERA: SATURNIIDAE)
J. MARK SCRIBER
Dept. ofEntomology, Michigan State University, East Lansing, Michigan 48824, USA
ABSTRACT.- Larval growth rates and efficiencies were measured using standard gravimetric techniques for penultimate and final instar North
AmericanAntheraeapolyphemusand AsianA. pernyisilkmoths to evaluateecological hypotheses about the physiological adaptations ofthese two
species. Contrary to expectations, the oak-feeding specialist, A. pernyi did not grow more efficiently nor more rapidly than the polyphagous A.
polyphemuswhen fed 5different Quercusspecies andPrunusserotina. Infact, theA. polyphemusgenerallygrew morerapidly inspiteofthe lower
nutritional quality (leaf water and nitrogen content) of their food, than was the case for A. pernyi. Several potential explanations are discussed,
including body sizeeffects.
KEYWORDS: Alaska, Asia, behavior, British Columbia, Canada, China, Fagaceae, genetics, herbivory, hostplants, Hymenoptera, larvae, Mexico,
Missouri,Nearctic, Noctuidae, NorthAmerica,nutrition, Papilio,Papilionidae,parasitoids,Pennsylvania,Rosaceae,Spodoptera,Trichogrammatidae,
USA.
Antheraeapolyphemus (Cramer), the polyphemus silkmoth, is 1954; Waldbauer, 1968; MacArthur, 1972; Scriber and Feeny,
probably the most widely distributed species of the North 1979). This hypothesis must beexamined at both the physiologi
American Satumiidae. Itoccurs across temperate North America cal (or metabolic) level and the genetic (or evolutionary) level
from the Gaspe Peninsula and British Columbia southward into beforethesignificanceofnegativegenetictradeoffsorphysiolog
Mexico (Ferguson, 1972). In addition to its wide geographical ical "costs" can be used to meaningfullyaddress suchan ecologi
range, it also may contend for the title of the most polyphagous cal presumption (Scriber and Ayres, 1988). While a few studies
of the North American silkmoths, with a reported food plant have attempted to specifically determine these assumptions, the
range of at least 50 hosts from more than 30 genera (Ferguson, data remain sparse and with mixed results for both individual
1972). physiological (Schoonhoven and Meerman, 1978; Scriber, 1978,
Antheraea pernyi (Guerin-Meneville), the Chinese oak (or 1981, 1986; Neal, 1987; Scriber and Dowell, 1991), and genetic
tussah) silkmoth, is an Asian relative of the North American A. (heritable) costs (Jaenike, 1990; Via, 1990; Thompson, 1994).
polyphemus.Thisspecies(A. pernyi)hasbeen bredandreared on Recently, studies of nicotine metabolism and detoxification cost
oak (Quercus spp.) (Fagaceae) in China for centuries, and (measured both by respirometry and E.C.D.'s) in two species of
recently has been used as the sourceofthe well-known Shantung Lepidoptera have shown that nicotine-adapted specialists have
(tussah) silk. This silk has been traced back to the Han dynasty little or no costs directly related to detoxication (Appel and
in China (206 B.C.-220 A.D.; Peigler, 1993). Martin, 1992) whereas the generalist Spodoptera eridania
While the North American A. polyphemus is extremely (Cramer) (Noctuidae) polysubstrate monoxygenase detoxication
polyphagous,itincludesatleast6-10oakspeciesas natural hosts. ofthis allelochemical does impose significantmetabolic costs on
In fact, it was suggested that A. polyphemus may still be beha the larvae (Cresswell et al., 1992).
viorally linked to theseancestral Quercus hostplants for success This study was conducted to determine if the physiological
ful mating (Riddiford, 1967; Riddiford and Williams, 1967). efficienciesofdigesting andconvertingfood tolarval body tissue
While often assumed that monophagy is the derived, and and/or the rate oflarval growth on a series ofhost plants would
polyphagy the ancestral condition (Brues, 1920, 1924; Dethier, be greater for the more specialized silk moth, Antheraeapernyi,
1954; Fraenkel, 1959; Ehrlich and Raven, 1964; Feeny, 1995), it than its polyphagous congenor, A. polyphemus. Presumably, the
appears that the generalist feeding behavior associated with the generalist A. polyphemus would exhibit greater metabolic loads
geographic spread ofA. polyphemus across North America and and lower efficiencies than the specialists. Five different oak
may have been derived from ancestral Asian oak-feeding (Quercus) species were included, since these are presumed to
specialists (Michener, 1952; Ferguson, 1972). represent the ancestral host plant favorites. Black cherry, Prunus
There has been a long-standing assumption that the efficiency seratina (Rosaceae), was included as a rosaceous outgroup yet a
(E.C.D.)and/orrate ofgrowth for a generalized feeder, would be natural North American host plant.
less on any given host plant compared to a specialist (Dethier,
24 SCRIBER: Antheraea Larval Growth HOLARCTIC LEPIDOPTERA
METHODS slightly underestimate true efficiencies because a small fraction
Cocoons of A. polyphemus were collected in Northhampton of nitrogen is excreted in the form of uric acid, allantoin,
Co., Virginia. Emerging adults were mated and confined to allantoic acid, or perhaps other compounds (Bhattacharya and
paperbags or plastic boxes with oak leaves for oviposition. We Waldbauer, 1972).
obtainedeggsin asimilarway forA. pernyiwhich were obtained The concern about uncritical use of nutritional ratios for
from captive cultures at Klingerstown, Pennsylvania, and St. interpretation of behavioral, physiological, and ecological
Louis, Missouri. Eclosing larvae were allocated in 6-10 groups implicationshas resurfaced recently, emphasizing newpointsand
into rearing containers each containing one of the foodplants several brought up as unresolved since earlier reviews (Wald
underexamination.Tominimizeanyeffectstolarvalconditioning bauer, 1968; Scriber and SIansky, 1981). The largest source of
(Jermy et ai., 1968) and host switching effects (Scriber, 1979, error in the gravimetric methodology for insects is generally in
1981, 1982; Stoyenoff et al., 1994) each group of larvae was estimating the food consumption: this can be due to difficulties
reared to the molt preceding the penultimate instar on the plant measuring small amounts eaten by early instars, fresh weight
species upon which the feeding experiment was to be conducted. variation among leaves and during the experiment, magnification
We do not know the host plant of the parents nor the potential ofmeasurementerrors, too much ortoo littlefood presented, and
maternal or paternal effects on offspring (Mousseau and Dingle, changes in foliage mass/composition during the experiment
1991). (AxelssonandAgren, 1979;GrabsteinandScriber, 1982;Schmidt
Each caterpillar used in the feeding experiments was weighed and Reese, 1986; Bowers et al., 1991; Stamp, 1991). Other
immediately after molting into the penultimate (and ultimate) complications remain even with the necessary use of dry mass
instarand transferred into its own clear plastic petri dish (15 cm budgets, sinceenergy content varies with lipid, protein, carbohy
diameter x 2.5 cm height), and provided a foodplant leaf of drates of insect and host plant (Gordon, 1968; Slansky and
known fresh weight. Eight larvae per plant species were used as Scriber, 1985; van Loon, 1991, 1993). Volatile lipids and highly
replicates in the penultimate instar, with 4-5 larvae used in the variable, or unrealistic caloric budgets can result from oven
final instar. Leaf petioles were inserted into water-filled, drying rather than freeze-drying the samples to be weighed.
rubber-capped plastic vials to maintain leaf turgor (see Scriber Comparisons of gravimetric and respirometric estimates of
1977). All dishes were then held in a large walk-in controlled metabolic efficiencies are useful and desirable (van Loon 1993),
environment chamber, maintained at a 16:8 photo-scoto-phase however are not always possible, as was the case here.
with corresponding day/night temperatures of 23°CII9°C and a Beyond some methodological sources of variation, one of the
relative humidity of 75 ± 10%. Unfortunately, the silkmoth recentconcerns involving nutritionalecology is the uncritical use
species were not available for precisely concurrent studies; of ratios and the statistical problems these may create. A series
however, identical procedures and analyses were conducted with of excellent reviews (Raubenheimer, 1995; Raubenheimer and
these slightly staggered bioassays during the same summer. Simpson, 1992, 1994; Simpson and Raubenheimer, 1995) has
Atintervalsof24-48 hours, eachcaterpillarwasreweighedand been modelled directly on previous examples (Atchley, 1978;
the feces and unconsumed leaf material were collected for Packard and Boardman, 1987, 1988) which were derived from
freeze-drying. Each caterpillar was replaced in the dish with a earlier statistical evaluations (e.g., Cochran, 1957). Common
new weighed leaf. A subset of 3-6 larvae were weighed live, terms in the "X" and "Y" variables (as in ratios) may lead to
frozen and freeze-dried to determine dry weight ratios. A subset spurious self-correlations, among other problems (see discussion
of 6-10 leaves for each experiment were similarly weighed at in Raubenheimer, 1995).
each replacement and dried for dry weight determination. Larval These studies were analyzed by plotting the efficiences (AD,
growth was measured as weight gained during the entire instar ECD, ECI)andrates (RCR, RGR) against themean larval weight
andstandardgravimetric methods (Waldbauer, 1968;Scriberand during each instar (the initial and final weight data were not
Slansky, 1981) were used to calculate the relative growth rates retained and were unavailable for using in the desirable analysis
(R.G.R.), efficiency of conversion of ingested (E.C.I.) and ofcovariance; Packard and Boardman, 1987, Raubenheimer and
digested food (E.C.D.), and approximate digestibility (A.D.). Simpson, 1992).
Larvae were weighed and set up immediately after molting to
avoid the incorrectattribution ofgutcontentto larval weightgain RESULTS AND DISCUSSION
(Bernays and Simpson, 1990; Barbehenn and Keddie, 1992). Theefficiency ofconverting digested food into larval biomass
In addition to dry weight ratios, the freeze-dried larvae, feces, (E.C.D.) was not significantly greater for penultimate instar A.
and leaves were stored in desiccators and later analyzed for pernyi (oak specialist)compared to the generalistA. polyphemus
caloric values and total nitrogen. Caloric contents were deter on any host plant species (Table la). In the final instar, only the
mined in triplicateinaPhillipson (1964) microbomb calorimeter. white oak treatment resulted in a significantly higher efficiency
Total nitrogen was measured from triplicate samples by the (E.C.D.) for A. pernyi than A. polyphemus. The same basic
micro-kjeldahl technique ofMcKenzie and Wallace (1954). This pattern is observed for E.C.I. (Table 1b). The mean relative
determination allowed calculation of the relative nitrogen growth rates (R.G.R.) of penultimate instar A. polyphemus
accumulation rate (RNAR; mg nitrogen gained per mg of larval generalists were also significantly greater than those of the
weightperday)andthenitrogenutilizationefficiency(NUE;ratio specialized A. pernyi on chestnut oak (Quercus prinus), red oak
of nitrogen gained to nitrogen ingested). These values for (Q. rubra), white oak (Q. alba), and black cherry (Prunus
efficiency ofconversion ofingested nitrogen into larval biomass seratina), with no significantdifference on swamp white oak (Q.
Vol. 3 No.1 1996 SCRIBER: Antheraea Larval Growth 25
TABLE la. Efficiencies of conversion of digested (E.C.D.) and lb. instars) was an explanatory correlation of relative growth rate
ingested (E.C.L) food to larval growth for penultimate and final instars observed with total leafnitrogen (% ofdry mass), caloricdensity
ofAntheraea moth species (data are presented as amean ± SE). (callmg), or leaf water content (% of fresh weight). In fact, the
Species Chestnut Red Swamp White Pin Black faster growth rates of A. polyphemus larvae, compared to A.
(andinstar) Oak Oak WhiteOak Oak Oak Cherry pemyi, were in spite ofgenerally lower leafwater contents (Fig.
E.C.D.(penultimateinstar) 1-2), which is also contrary to general observations for immature
insects (Scriberand Slansky, 1981) and tree-feeding Lepidoptera
pernyi 74.4(4.4) 42..2(2.8) 41..2(3.8) 40..9(1.5) 29.3(3.2) 17.2(3.0)
polyphemus 62.5 (2.9) 81.6(8.6) 63.5(4.8) 834(6.1) 33.0(29) 14.3(8.9) in particular (Mattson and Scriber, 1987). In addition, for most
(F·ratio) (N.S.) ( ) ( ) ( ) (N.S.) (N.S.) hostplantpairstheleaves wereslightly lowerin total nitrogen for
E.C.D.(finalinstar) thegeneralistA. polyphemusthan forA. pernyi(Fig. 1-2).Caloric
pernyi 23..8(1.2) 11.7(1.6) 14.7(1.4) 23..4(0.4) 17.1 (4.7) density of plant leaves ranged from 4.8 to 5.2 callmg and were
pol)phemus 54.7(11.8) 10.3(5.9) 34.7(8.6) 17.1 (1.7) 29.7(5.0) not correlated with any index oflarval growth or efficiency.
(F-ratio) ( ) (N.S.) (N.S.) ( ) (N.S.)
The poorer performance of A. pemyi on 5 Quercus species,
TABLE lb. compared to A. polyphemus, was unexpected based on the
assumption that a polyphagous "super-generalist" would be less
Species Chestnut Red Swamp White Pin Black
(andinstar) Oak Oak WhiteOak Oak Oak Cherry efficient than the oak specialized species. This exceptional
performance of A. polyphemus larvae was not due to belter
E.C.I.(penultimateinstar)
nutritional leafquality, which was the case for A. pemyi larvae.
pernyi 20..3 (0.6) 12..4(0.5) 15..4(0.5) 1.62(06) 8.7(0.4) 8.1 (08)
In fact, the A. pernyi hosts were of higher nutritional quality.
poLyphemus 14.1 (0.7) 22.2(1.4) 18.7(1.0) 18.5(0.6) 7.9(0.5) 7.4(2.6)
(Fratio) ( ) ( ) ( ) ( ) (N.S.) (N.S.) Perhapstheexplanationofpoorerlarvalconversionefficiencyand
E.C.1.(finaiinstar) growth performance ofA. pernyi is simply that these particular
pernyi 8..6(0.5) 3.6(0.5) 4..9(05) 10..8(0.4) 4.7 (1.0) host plant species are not their ancestral Quercus species. An
polyphemus 11.5(0.5) 8.9(3.5) 10.7(2.0) 6.0(0.7) 6.9(1.0)
apparent lack of specific physiological adaptations for efficient
(Fratio) ( ) (N.S.) ( ) ( ) (N.S.)
metabolic processing of North American trees may be due to
•Significantdifferencesbetweenthemeansareindicated(.)althep=0.05level(Snedecor insufficient timesince therecentimportationofA. pemyiinto the
andCochran, 1967).N.S. = non·signiticance. USA (brought in during the last couple of decades by lepidop
terists, research physiologists, and biological control specialists
TABLE2. Relativegrowth rates (mg. mg-I . d·l) oftwoAntheraea moth formass-rearingofTrichogramma (Hymenoptera:Trichogramma
specieson six host plant species. tidae) egg parasitoids for use against forest pestspecies; Peigler,
1993).
Host PlantSpecies
While the efficiency of assimilating and converting tree leaf
Species Chestnut Red Swamp White Pin Black biomass to insect herbivore biomass and the subsequent rate of
(andin,tar) Oak Oak WhiteOak Oak Oak Cherry larval growthisdetermined primarily by the nutritional quality of
R.G.R.(penultimate) the food (Scriber, 1984; Mattson and Scriber, 1987; Slansky,
pernyi .1.6(.00) .1.8(.Ot) .18(.01) .1.6(.01) .16(.01) .0.4(.01) 1992, 1993), we did not observe this to be the case with these
pol)phemus .19(.01) .23(.02) .18(.01) .22(.01) .14(.01) .07(.01) oak-feeding silk moths. In fact, a weak but negative correlation
(Fratio) ( ) ( ) (N.S.) ( ) (N.S.) ( ) of penultimate instar growth rate (RGR) and leaf water content
R.G.R.(finalinstar) was observed (Fig. la). Quercus leafnitrogen concentrations are
perny; .0.5(.01) .0.3(.01) .0.5(.00) .05(.00) .0.3(.00) also less for the fast-growing generalists on every oak species in
polyphemus .10(.01) .06(.01) .10(.00) .07(.01) .07(.01) both instars (Fig. Ib-2b).
(Fratio) ( ) ( ) ( ) (N.S.) ( )
Metabolic costs ofdetoxification will depend on the specific
•Significantdifferencesbetweenthemeansareindicated(.).p==0.05level. mechanisms involved and the affiliated evolutionary adaptations
bicolor) or pin oak (Q. palustris; Table 2). The final instar A. ofeach herbivore in question. For example, one allelochemical,
polyphemus larvae also grow faster than A. pemyi larvae on all nicotine, is metabolically costly for the polysubstrate oxygenase
5oakspecies, although this does notreach significance for white detoxication system of a generalist caterpillar (Cresswell et al.,
oak (Table 2). 1992) but specialist caterpillar species with rapid excretion
abilities and target site insensitivity has insignificant metabolic
These results indicate that the extremely polyphagous North
costs for detoxification (Appel and Martin, 1992). Perhaps these
American silkmoth, A. polyphemus, is both more efficient and
differences in mechanisms of detoxication with differential
morerapid in larval growth than theA.pernyioakspecialist.This
associated metabolic costs explain the mixed results in past
is precisely the opposite result that ecological theory might
attempts to quantify differences for specialist insects and genera
predictbased simply on the assumption thatthe morespecialized
list insects since Krieger et al. (1971) and Whittaker and Feeny
A.pemyilarvaewould bemoreefficientatconversionona given
(1971) suggested that selection for detoxification energy effi
host than would larvae of their generalized congenors, A.
ciency would be expected in specialists compared to generalists
polyphemus. To determine if the larval performance of A.
(which were presumed to have agreater numberofdetoxification
polyphemuswastheresultofhostnutritionaldifferences, analyses
systems to maintain and operate as a "metabolic load"; Slansky,
ofthe leaves were conducted independently for each species and
1993). While the North American generalistA. polyphemus is
each instar on every host plant. In no case (penultimate or final
26 SCRffiER: Antheraea Larval Growth HOLARCTIC LEPIDOPTERA
Final Instar
Penultimate Instar
.24
'0 .12 be
wo
co
swo_______ RO swo 5\\10 CO
.16 PO~
.08
"0 "0
po wo
00 00
E E '0
--
.08 co wo swo
be .04
00 00
E BC E po RO
..C.l.J 58 62 66 70
r;:
c:::: 54 58 62 66 70 Leaf Water Content (% )
.: Leaf Water Content (% )
.12
be
~ .24
.0... '0
wo co swo
l?
co
..;.C->.l.J .16 po Rq,wo SWO .08
- COWO po wo
r;:
Po ro
ClJ
c:::: co wo SWO
.04
.08 po RO
be
BC 1.0 2.0 3.0 4.0
Total Leaf Nitrogen (%)
I~ 4~ Fig. 2. The relative growth rates of final instar Antheraea pernyi and A.
polyphemus on various hosts as a function of leaf water (r = 0.12) and leaf
Total Leaf Nitrogen (%) nitrogen content(r=0.06)(same codingas inFig. I).
Fig. 1. The relative growth rates of penultimate instar larvae (mg·mg-'·d·') of forsizeinattemptingtoassessthetissuegrowthrates (Waldbauer
Antheraeapernyi(largeletters)andA.polyphemus(smallletters)onChestnutoak 1968). This and related statistical problems described recently
(co), Red oak(ro), Swamp whiteoak(swo), White oak(wo), Pinoak(po), and
(Raubenheimer and Simpson, 1992, 1994; Raubenheimer, 1995)
Blackcherry(be) as afunction ofleafwatercontent(percentfresh weight; top,
led to an evaluation of raw data for all of the A. pemyi and A.
r=0.40)andtotal nitrogen (percentdry weight; bottom, r=0.21).
polyphemus comparisons with regard to their size differences.
believed to be derived from the Asian oak specialists (e.g., a
The A. polyphemus larvae were generally smaller than A.
proto-pemyi; Ferguson, 1972), wesee no evidence that there has
pemyi in both the penultimate and final instars. This was most
been any loss of efficiency or growth rate in this polyphagous
pronounced for larvae on chestnut oak and pin oak (Tables 3-4).
derivative and ifanything, they do better on nutritionally poorer
While mean size (B) is not included in the calculation of the 3
hosttissues. No simple explanation is availablefor such atypical
efficiencies (AD, ECD, orECI), itcertainly could have an effect,
results (Slansky and Scriber, 1985).
due to a smaller gut surface area relative to body weight for
BODY SIZE EFFECTS example. However, the increasedvolume ofgutepithelialcellsin
Body size can have major significance in the feeding ecology larger larvae (rather than surface area of the lumen) may have
ofLepidoptera (Scriberand Slanksy, 1981; Mattson and Scriber, equalizing effects on the assimilation efficiency (Reavy, 1993).
1987;Reavy, 1993).Theinitialsizecan beofprimaryimportance When plotted against the average size during the penultimate
for establishment on the host plantand in successful completion and final instarsofbothspecies,thereis nosignificantinteraction
ofa given generation in certain thermally constrained situations, ofmean weight with the approximatedigestibility (AD)and only
as described for Papilio in Alaska (Ayres and Scriber, 1994). It a slight hint of an effect in the final instar for the conversion
is clearthatbiggerlarvaeeatmore and analysis ofgeneral trends efficiency of digested food (ECD), but the overall conversion
in nutritional indices indicate that with more food eaten, more efficiency of ingested food (ECI =AD X ECD) shows no size
weight is gained, but lower relative consumption rates and effect for either instar (Fig. 3).
relative growthrates existfor largerlarvae (laterinstars; Siansky In contrast, the relative consumption rates (RCR) and the
and Scriber, 1985; Reavy, 1993). Use ofratios in calculating the relative growth rates (RGR) ofA. polyphemus and A. pemyi do
RGR(weightgained/meanweight·d)may notadequatelycorrect show an effect ofaverage size in the final instar (but not the
Vol. 3 No.1 1996 SCRIBER: Antheraea Larval Growth 27
2.00,------- ---,
TABLE 3. Penultimate instar weight gain and mean weight during the
instarfor different host species. Data are presented as a mean (±SE).
•
Biomassincrease(mgdry) Averageweight
(mgdry)
(n) polyphemus (n) pernyi polyphemus pernyi
1.50
ChestnutOak (6) 125± II (8) 452± 14 107±6 439± 14
RedOak (5) 360± 12 (8) 363± 18 292±4 313±9 •
SwampWhileOak (6) 263± 15 (5) 301 ± 14 235± 11 256± 8 I:l::
PWinhiOteakOak ((65)) 213890±± 1174 ((88)) 331819±±2234 2t8092±± 1182 329239±±2107 UI:l:: •• 0 o
BlackO1erry (2) 120± 29 (4) 167± 15 136±24 215±9 0
1.00 •• ~ 0@] @]
TABLE4.Finalinstarweightgainandmeanweightsduringtheinstarfor
0
different host species. Data are presented as a mean (±SE).
[QJ [QJ
Biomassincrease(mgdry) Averageweight
(mgdry) o.so+----I-"l'J,------,-----.,---4~Ql~------1
o 250 500 750 1000 1250
(n) polyphemus (n) pernyi polyphemus pernyi
ChestnutOak (4) 505± 92 (4) 849± 28 460±60 1066±36 MEAN MASS
RedOak (3) 557± 173 (4) 388± 36 770± 87 683± 32
SwampWhileOak (4) 557± 14 (4) 524±45 666±71 823±40 Fig.4.The relativeconsumptionrate (R.C.R.= mgingested/mg·d; dry weight
WhiteOak (4) 342± 108 (4) 739±46 476±65 963± 60 basis)as a function ofaverageweightoflarvae ofA.polyphemusandA.pemyi
PinOak (4) 560± 105 (4) 478± 35 695±96 836± 61 during the penultimate and final instars on 5 oak species and black cherry.
·BlackCherry (I) 441 (-) 376
Symbolsaredescribed in Fig. 3caption.
*Poorsurvivalinthefinalinstar(onlyonelarvacompleteddevelopment).
0.25
penultimateinstar;seeFig. 4-5). Unfortunately, theinitial weights •
•
andfinal weights oflarvaeforeachinstarwere notretained (after
the weight gained and the average weights were calculated), and 0.20-
•
therefore, it is not possible to do the desired analysis of covar
~OO
iance(PackardandBoardman, 1987;RaubenheimerandSimpson,
~ 00
1992; Horton and Redak, 1993). Even if these values were 0.15
•
available, they might not be useful since the instar weights for I:l::
each hostplanttreatment were influenced by previous feeding on ~ 0
I:l::
that host and not randomly assigned across host treatments. 0.10 0 0
What is clearis that ratio transformation ofconsumption rates
•
and growth rates by mean sizedo notentirely remove the effects 0 0
0
ofsize for the final instars. It appears that a general size-related 0.05· [QJ [QJ @]
00
25-,-------------- ----, [Q] @]
•
0.00 ,
20 00 0 250 500 750 1000 1250
••
MEAN MASS
0000
15 Fig.S.The relativegrowth rate (R.G.R.= mg gained/mg· d; dry weight basis)
• as afunction ofaverageweightofthelarvaeduringeach instar(seecaptionFig.
u
00 3).
'" 0
10 0 @]
difference between A. pernyi and A. polyphemus relative growth
00 0 0 @]
.@1 rate and relative consumption rate (not efficiency) exists in the
0
0 final in5tar stage. This could indicate that for every host species
5- @ except red oak (where A. pernyi is smaller than A. polyphemus),
@]
the smallerA. polyphemus appear to consume food faster (RCR,
Fig. 4) and grow faster (RGR, Fig. 5) simply because of their
0 . .
0 250 500 750 1000 1250 size, and not because of their adaptations for processing North
American species of tree leaves. This conclusion might also be
MEAN MASS reached in pairwise comparisons of penultimate instars for
Fig.3.Theoverallefficiencyofconversionofingestedmassintolarvalbiomass chestnut oak, white oak, and black cherry (but not swamp white
gain(E.c.I. =A.n. xE.c.n.)as a function ofaveragesizeoflarvae in penulti oak or pin oak; Fig. 5). However on red oak the mean size is the
mateandfmal instars.Solidsymbolsrepresentpenultimateinstars.opensymbols
same but the growth rate ofA. polyphemusis significantlyhigher
arefinal instars. LargesquaresareA.pemyi; the small areA.polyphemus.
than A. pernyi (see Tables 2-3).
28 SCRIBER: Antheraea Larval Growth HOLARCTIC LEPIDOPTERA
WhyA. polyphemus is smaUer than A. pemyi may be ecologi REFERENCES
cally more significant than the possibility that they are able to
consumeandprocessNorthAmericanhosts forfastergrowththan Appel, H. M., and M. M. Martin
are their Asian congenors. For example, if the seasonal degree 1992. The significance of metabolic load in the evolution of host
day (thermal) accumulations for these A. polyphemus source specificityofManduca sexta(Lepidoptera: Sphingidae). Ecol.
(New York), 73:216-228.
populations are restrictive, smaller size may allow completion of
Atchley, W. R.
thegeneration. Ithas previously beensuggested that small sizeof
1978. Ratios, regression intercepts. and the scaling of data. Syst.
adults is selected for in such thermally constrained areas (Ayres
Zool. (Washington), 27: 67-71.
and Scriber, 1994; Scriber, 1994, 1996). It is also important to
Axelsson, B.,and G. I. Agren
understand the entire environment on the larval performance of 1979. Acorrectionfor food respiration in balancingenergy budgets.
any species. Natural photoperiods or thermoperiods may cue a Ent. Exp. Appl. (Amsterdam), 25: 260-266.
caterpillar's behaviorand affect its physiological performanceon Ayres, M. P., and S.F. MacLean
different species with different allelochemicals (Scriber and 1987. Molt as a component of insect development: Galerucella
Siansky, 1981; Slansky, 1992; Matsuki and MacLean, 1994; sagittarae (Chrysomelidae) and Epirrita autumna (Geometri
Stamp, 1994a, 1994b). Other variables of potential ecological dae) Dikos (Copenhagen), 48: 273-279.
significance that were not measured in this study include: I) the Ayres, M. P., and J. M. Scriber
egg sizeofthe two silkrnoths, 2) the duration ofthe molt (which 1994. Local adaptations to regional climates in Papilio canadensis
(Lepidoptera: Papilionidae). Ecol. Monog. (Durham, NC), 64:
insometemperatures islongerthan theinstarduration; Ayresand
465-482.
MacLean, 1987; Ayres and Scriber, 1994).
Barbehenn,R. V., and A. Keddie
Since solittleis known aboutthe ecology ofA.pernyi in Asia,
1992. Gut contents in molting lepidopteran larvae: asourceoferror
it is with greatcaution thatcomparisons ofnutritional physiology
innutritionalstudies. Ent. Exp. Appl.(Amsterdam),62: 87-91.
must beconsidered. For example, ifAsian Quercus host species Bhattacharya, A. K., and G. P. Waldbauer
are allelochemically very different as a group than the five North 1972. Theeffectofdietonthenitrogenous end-productsexcretedby
American species used in thesecomparativebioassays,onemight larval Tribolium confusum: with notes on the correction of
hypothesize that the biochemical detoxication mechanism ofthe A.D. andE.C.D. for fecal urine. Ent. Exp. Appl. (Amsterdam),
Asian oak-feeding A. pemyi is inefficient on the American host 15:238-247.
species; however, suchspeculationis notjustified.Weknowlittle Bowers,M. D., N. E. Stamp,and E. D. Fajer
1991. Factors affecting calculation of nutritional indices for fo
aboutthephytochemistryofAsian oaksin regard toinsecttoxins,
liage-fed insects; an experimental approach. Ent. Exp. Appl.
deterrents and nutrients, or their interactions (butseeGavrilchik,
(Amsterdam), 61:101-116.
1991). Also, the five American oak species used in these studies
Brues, C. T.
can have significant differences in gallotannins, total phenolics,
1920. The selection offoodplants for insects, with special reference
foliarastringency,andproanthocyanidins(Hunter, 1994).Itwould
to lepidopterous larvae. Amer. Nat (Salem), 54:313-332.
seem logical that such differences among these North American 1924. Thespecificityoffoodplants in theevolutionofphytophagous
Quercus species would elicit differential interspecific larval insects. Amer. Nat. (Salem), 58:127-144.
growth efficiencies or growth rates ifdifferential adaptations (or Cochran, W. G.
"exaptations"; Lauder et ai., 1993) existed for these silkmoths. 1957. Analysis of covariance: its nature and uses. Biometrics
Perhaps the only way to evaluate the differential Quercus (Raleigh), 13:261-281.
chemistry hypothesis would be to test both Antheraea species Cresswell,J. E., S. Z. Merritt,and M. M. Martin
1992. The effect ofdietary nicotine on the allocation ofassimilated
concurrently on Asian oaks to see if the larval growth perfor
food to energy metabolism and growth in fourth-instar larvae
mances are reversed.
of southern armyworm, Spodoptera eridania (Lepidoptera:
Although the few larvae that died during these studies did not
Noctuidae). Decologia (Berlin), 89:449-453.
look to be diseased, it is certainly feasible that other sub-lethal
Dethier, V. G.
pathogen influences were, for unknown reasons, more prevalent
1954. Evolution of feeding preferences in phytophagous insects.
in A. pemyi than A. polyphemus. Such differences in microbial Evol. (Lancaster, Pal, 8:33-54.
susceptibility deserve additional study, since microbe/plant! Doucet, C. M., and J. P. Ball
herbivore interactions are very poorly understood yet may be 1994. Analysis ofdigestion data: apparent and true digestibility of
responsible in part for significant differences in population foods eaten by beavers. Amer. Midl. Nat. (Notre Dame), 132:
responses and maternal effects (Mousseau and Dingle, 1991; 239-247.
Rossiter, 1994; Scriber and Haas, 1996). Ehrlich, P. R., and P. H. Raven
1964. Butterflies and plants: astudy in coevolution. Evol. (Lancas
ACKNOWLEDGEMENTS ter, Pal, 18:586-608.
Feeny, P.
1995. Ecological opportunism and chemical constraints on the host
This work was supported in part by the Agricultural Experi
associations of swallowtail butterflies. In 1. M. Scriber, Y.
ment Stations at Michigan State University and Cornell Univer
Tsubaki,andR. C. Lederhouse(eds.),SwallowtailButterflies:
sity. I want to thank Dan Herms for his elucidation of the size Their Ecology and Evolutionary Biology, 9-16. Gainesville:
effects and statistical concerns with ratios. Sci. Pub!.
Ferguson, D. C.
Vol. 3 No.1 1996 SCRIBER: Antheraea Larval Growth 29
1972. The Moths of America North of Mexico. Fasicle 20.2B. Michener, C. D.
Bombycoidea: Satumiidae (in part). London: E. W. Classey 1952. The Saturniidae (Lepidoptera) of the Western Hemisphere:
and RB.D. Pub\. 275pp. Morphology phylogeny and classification. Bull. Amer. Mus.
Fraenkel, G. S. Nat. Hist. (New York), 98:335-502.
1959. The raisond'etreofsecondaryplantsubstances. Science (New Mousseau, T. A., and H. Dingle
York), 129:1466-1470. 1991. Maternal effects in insect life histories. Ann. Rev. Ent. (Palo
Gavrilchik, Z. S. Alto), 36:511-534.
1991. Energeticsoffeedingofthechinaoakworm(Antheraeapemyi Neal, J. J.
G) caterpillar at different temperatures. Zh. Obshch. BioI. 1987. Metabolic costs of mixed-function oxidase induction in
(Moscow), 52:82-88. Heliothis zea. Ent. Exp. Appl. (Amsterdam), 43:175-179.
c.,
Gordon, H. T. Packard, G. and T. J. Boardman
1968. Quantitative aspects ofinsect nutrition. Amer. Zool. (Utica), 1987. The misuse of ratios to scale physiological data that vary
8:131-138. [In Russian] allometrically with body size. In M. E. Feder, A. F. Bennett,
Grabstein,E. M., and J. M. Scriber W. W. Burggren, and R B. Huey (eds.), New Directions in
1982. Therelationshipbetween restriction ofhostplantconsumption EcologicalPhysiology. Cambridge: Cambridge Univ. Pr.
and post-ingestive utilization of biomass and nitrogen in 1988. The misuse of ratios, indices, and percentages in
Hyalophora cecropia. Ent. Exp. Appl. (Amsterdam), 31: ecophysiological research. Physiol. Zool. (Chicago), 61:1-9.
202-210. Peigler, R. S.
Horton, D. R., and R. A. Redak 1993. Wild silks of the world. Amer. Ent. (Philadelphia), 39:
1993. Further comments on analysis ofcovariance in insect dietary 151-161.
studies. Ent. Exp. Appl. (Amsterdam), 69:263-275. Phillipson,J.
Hunter, M. D. 1964. A miniature bomb colorimeter for small biological samples.
1994. The search for pattern in pest outbreaks. In S. R Leather, A. Oikos (Copenhagen), 15:130-139.
D. Watt, N. J. Mills, and K. F. A. Walters (eds.), Individuals, Raubenheimer, D.
Populations and Patterns in Ecology, 433-435. Hampshire: 1995. Problems with ratio analysis in nutritional studies. Funct.
Andover. Ecol. (Oxford), 9: 21-29.
Jaenike, J. Raubenheimer, D.,and S.J. Simpson
1990. Host specialization in phytophagous insects. Ann. Rev. Ecol. 1992. Analysis of covariance: an alternative to nutritional indices.
Syst. (Palo Alto), 21:243-273. Ent. Exp. Appl. (Amsterdam), 62:221-231.
Jaenike, J. 1994. The analysis of nutrient budgets. Funct. Ecol. (Oxford),
1994. Host specialization in phytophagous insects. Ann. Rev. Ecol. 8:783-791.
Syst. (Palo Alto), 21:243-273. Reavey, D.
Jermy, T.,F. E. Hanson, and V. G. Dethier 1993. Why body size matters to caterpillars. In N. C. Stamp and T.
1968. InductionofspecificfoodpreferencesinLepidopterouslarvae. Casey (eds.), Caterpillars: Ecological and Evolutionary
Ent. Exp. Appl. (Amsterdam), II:211-230. Constraints on Foraging, 248-279. New York: Chapman and
Krieger, R. r., P. P. Feeny, and C. F. Wilkinson Hall. 587pp.
1971. Detoxicationenzymes in thegutsofcaterpillars: an evolution Riddiford, L. M.
ary answer to plant defenses? Science (New York), 171: 1967. Trans-2-hexanal: mating stimulant for polyphemus moths.
579-581. Science (New York), 158:139-141.
Lauder,G. V., A. M. Leroi, and M. R. Rose Riddiford, L. M., and C. M. Williams
1993. Adapta~ions and history. Trends Ecol. Evol. (Cambridge), 1967. Chemical signaling between polyphemus moths and between
8:294-297. moths and the host plant. Science (New York), 156:541.
Loon, J. J. A. van Rossiter, M. C.
1991. Measuring food utilization in plant-feeding insects - toward a 1994. Maternal effects hypothesis of herbivore outbreak. BioSci.
metabolic and dynamic approach. In E. Bernays (ed.), (Washington), 44:752-763.
Insect-Plant Interactions, 3:79-124. BocaRaton: CRC Pro Schmidt, D. J., and J. C. Reese
1993. Gravimetric vs. respirometric determination of metabolic 1986. Sources of error in nutritional index studies of insects on
efficiency in caterpillars ofPieris brassicae. Ent. Exp. Appl. artificial diet. 1. Insect. Physiol. (London), 32:193-198.
(Amsterdam),67:135-142. Schoonhoven, L. M., and J. Meerman
MacArthur, R. H. 1978. Metabolic cost of changes in rliet and neutralization of
1972. Geographical Ecology. New York: Harperand Row. 269pp. allelochemics. Ent. Exp. Appl. (Amsterdam), 24:489-493.
Matsuki, M., and S.F. MacLean Scriber,J. M.
1994. Effects of different leaf traits on growth rates of insect 1977. Limiting effects of low leaf-water content on the nitrogen
herbivores on willows. Oecologia (Berlin), 100:141-152. utilization, energy budget, and larval growth of Hyalophora
Mattson, W. J., and J. M. Scriber cecropia (Lepidoptera: Satumiidae). Oecologia (Berlin), 28:
1987. Nutritionalecologyofinsectfolivores ofwoodyplants: water, 269-287.
nitrogen, fiber, and mineral considerations. In F. Slansky, Jr., 1978. CyanogenicglycosidesinLotuscorniculatus:theireffectsupon
and J. G. Rodriguez (eds.), Nutritional Ecology of Insects, growth, energy budget,andnitrogen utilizationin thesouthern
Mites, andSpiders, 105-146. New York: J. Wiley. armyworm, Spodoptera eridania. Oecologia (Berlin), 34:
McKenzie, H. A., and H. S. Wallace 143-155.
1954. The Kjeldahl determination of nitrogen: a critical study of 1979. The effectofsequentially switching foodplants upon biomass
digestion conditions - temperature, catalyst, and oxidizing and nitrogen utilization by polyphagous and stenophagous
agent. Aust. J. Chem. (Melbourne), 7:55-70. Papilio larvae. Ent. Exp. Appl. (Amsterdam), 25: 203-215.
30 SCRIBER: Antheraea Larval Growth HOLARCTIC LEPIDOPTERA
1981. Sequential diets, metabolic costs, and growth of Spodoptera Snedecor, G. W., and W. G. Cochran
eridania(Lepidoptera:Noctuidae)feedingupondill,limabean, 1967. Statistical Methods. Ames: Iowa St. Univ. Pro 593pp.
and cabbage. Oecologia (Berlin) 51:175-180. Stamp,N. E.
1982. Thebehaviorandnutritionalphysiologyofsouthernarmyworm 1991. Stabilityofgrowth and consumption rates and food utilization
larvae as a function of plant species consumed in earlier efficiencies when insects are given an excess of food. Ann.
instars. Ent. Exp. Appl. (Berlin), 31:359-369. Ent. Soc. Amer. (Lanham), 84:58-60.
1984. Insect!PlantInteractions - Host plant suitability. pp. 159-202 1994a. Interactive effects of rutin and constant versus alternating
In W. Bell and R. Carde (eds.), The Chemical Ecology of temperatures on performance of Manduca sexta caterpillars.
Insects, 159-202. London: Chapman and Hall. Ent. Exp. Appl. (Amsterdam), 72:125-133.
1986. Originsoftheregional feeding abilitiesinthetigerswallowtail 1994b. Simultaneous effects of potassium, rutin, and temperature on
butterfly: ecological monophagy and the Papilio glaucus performance of Manduca sexta caterpillars. Ent. Exp. Appl.
australissubspeciesinFlorida. Oecologia(Berlin),71:94-103. (Amsterdam),72:135-143.
1994. Climaticlegaciesandsexchromosomes: latitudinal patternsof Stoyenoff,J.L.,J.A.Witter,M.E.Montgomery,and C.A.Chilcote
voltinism, diapause size and host-plant selection in 2 species 1994. Effects of host switching on gypsy moth (Lymantria dispar
ofswallowtail butterfliesat theirhybrid zone. In H. V. Danks (L.) under field conditions. Oecologia (Berlin), 97:143-157.
(ed.), Insect Life-Cycle Polymorphism: Theory, Evolution and Thompson,J. N.
Ecological Consequences for Seasonaliry and Diapause 1994. The Coevolutionary Process. Chicago: Univ. ChicagoPr. 376
Control, 133-171. Dordrecht: Kluwer Academic Publ. pp.
1996. Anew coldpockethypothesis toexplainlocal hostpreference Via, S,
shifts in Papilio canadensis. Ent. Exp. Appl. (Amsterdam), [in 1990. Ecological genetics and host plant adaptations in herbivorous
press]. insects: the experimental study of evolution in natural and
Scriber,J. M., and M. P. Ayres agricultural systems. Ann. Rev. Ent. (Palo Alto), 35:421-466.
1988. Leaf chemistry as a defense against insect herbivores. In Waldbauer, G. P.
AnimalandPlantSciences, 1:117-123. Inst. ScientificInform. 1968. The consumption and utilization offood by insects. Adv. Ins.
Scriber,J. M., and R. Dowell Physiol. (London), 5:229-288.
1991. Host plant suitability and a test of the feeding specialization Whittaker, R, H., and P. P. Feeny
hypothesis using the giant swallowtail butterfly Papilio 1971. Allelochemics:chemicalinteractionsbetweenspecies. Science
cresphontes. GreatLakes Ent. (East Lansing), 24: 27-37. (New York), 171:757-770.
Scriber,J. M., and P. P. Feeny
1979. Growth of herbivorous caterpillars in relation to feeding
specialization and to the growth form of their food plants.
Ecol. (New York), 60: 829-850.
Scriber,J. M., and L. Haas
1996. Long term effectsofB.t.k. on non-target Lepidopteraspecies,
andpotentialcausal mechanisms.Proc. Natl. GypsyMothRev.
(TraverseCity, Mi): [in press].
Scriber,J. M., and R. C. Lederhouse
1992. The thermal environment as a resource dictating geographic
patterns offeeding specialization ofinsect herbivores. In M.
R. Hunter, T. Ohgushi, and P. W. Price (eds.), Effects of
ResourceDistribution onAnimal-Plant Interactions, 429-466.
New York: Acad. Pr.
Scriber,J. M., and F. Slansky,Jr.
1981. The nutritional ecology of immature insects. Ann. Rev. Ent.
(Palo Alto), 26:183-211.
Simpson,S.J., and D. Raubenheimer
1995. Thegeometricanalysisoffeeding andnutrition: auser'sguide.
J. Ins. Physiol. (London), 41:545-553.
Slansky, F.,Jr,
1992. Allelochemical-nutrient interactions in herbivore nutritional
ecology. In G. A. Rosenthal and M. R. Berenbaum (eds.),
Herbivores: Their interactions with secondary plant metabo
lites, 2. Ecological and Evolutionary Processes, 135-174. (2nd
ed.). New York: Academic Press.
1993. Nutritional ecology: The fundamental quest for nutrients. In
N. E. StampandT. M. Casey(eds.), Caterpillars: Ecological
andEvolutionaryConstraintson Foraging, 29-91. New York:
Chapman & Hall.
Slansky,F.,Jr., and J. M. Scriber
1985. Food consumption and utilization. In G. A. Kerkut, and L. I.
Gilbert(eds.),ComprehensiveInsectPhysiology,Biochemistry,
andPharmacology, 4:87-163. Oxford: Permagon Press.
