Ecological Entomology (199 I) 16, 1-9

The effect of host-plant quality on the survival of larvae and oviposition by adults of an ant-tended lycaenid , evagoras

M. BAYLIS and N. E. PIERCE* Department of Zoology, University of Oxford, and *Department of Biology, Princeton University

Abstract. 1. Juveniles of the Australian lycaenid butterfly, Jalmenus evagorus (Donovan), secrete to ants a solution of sugars and amino acids, primarily serine. The attendant ants protect the larvae and pupae from parasites and predators. 2. The effect of caterpillar nutrition on the defence provided by ants was investigated. Potted food plants of decurrens were either given water containing nitrogenous fertilizer or were given water alone. Fertilized plants had a higher nitrogen content than unfertilized plants. 3. Fifth instar larvae of J.evagoras feeding on fertilized plants attracted a larger ant guard than those feeding on unfertilized plants. In the absence of caterpillars, ants were not differentially attracted to fertilized and unfertilized plants. 4. In the presence of ants, over a 10-day period, larvae on fertilized plants survived better than larvae on unfertilized plants. In the absence of ants larvae survived equally on fertilized and unfertilized plants. It is concluded that larvae on fertilized plants attracted a larger ant guard, and thereby survived better, than larvae on unfertilized plants. 5. Adult females of J.evugoras preferred to lay egg batches on ferti- ized, rather than unfertilized plants, but they did not lay larger egg batches.

Key words. Host-plant quality, nitrogenous fertilizer, oviposition, ant attendance, , , .

Introduction a range of food plant species or populations and usually higher nitrogen levels have been There have been many investigations of the found to increase survival (Myers & Post, 1981; effect of nitrogen levels of food plant on the Myers, 1985; Ohmart etal., 1985; Taylor, 1988), survival of phytophages. The nitrogen level of although in some studies increases in nitrogen food plants has generally been varied by the have been found to have no effect (Lincoln, application of fertilizer or by sampling from 1985; Ohmart et al., 1985) or even a negative effect (Stark, 1965; Myers, 1985). Since nitrogen Correspondence: Dr M. Baylis, Tsetse Research and water levels are often correlated in plants Laboratory, Department of Vctcn nary Sciences, (Seriber & Slansky, 1981), it is difficult to separ- Langford House, Langford, Bristol BS18 7DU. ate their effects (and, indeed, those of any

1 2 M. Buylis arid N. E. Pierce other factors which change concentration with plants, apart from possibly gaining a direct the application of fertilizer or between plant nutrition-related increase in survival for the species or populations) on phytophage survival. reasons described above, might additionally This has been overcome in some studies by the gain an increase in survival via an cnhanced use of artificial diets. Increasing the protein ability to attract ants. In other words, by pro- content of artificial diets while holding water ducing a larger volume of secretion, or providing content constant has been shown to increase secretion with a higher concentration of nu- survival (Lincoln eta/., 1982; Cates et al., 1987) trients, caterpillars of J.evagoras might be able although the effect may depend on the type of to attract more ants for defence and thereby protein used (Johnson & Bentley, 1988). survive better. Phytophages have developed numerous Here we describe experiments which inves- mechanisms that enable them to take advantage tigate the effect of host plant quality. varied by of nitrogen and water-rich (more 'nutritious') the application of nitrogenous fertilizer, on the food (Simpson & Simpson, 1991)). For example, attractiveness of larvae of J.evagora.s to ants, the feeding stage of some may exhibit the survival of the larvae in the wild, and finally facultative carnivory, feed on the most nitrogen- the ovipositional responses of adult females of rich plant part, change position or plant with J.evagorus to higher and lower quality larval season and may alter host plant chemistry food plants. (McNeill & Southwood, 1978; Mattson, 1980). Furthermore, insects on nutritionally poor diets may maximize their nutrient uptake by in- creasing feeding rates or development time Materials and Methods (Simpson & Simpson, 1990; Taylor, 1989). Female insects may also selectively oviposit on Natural history and study sites. J. c'vugoras is plants most nutritionally suitable for their off- a multivoltine, Australian lycaenid butterfly that spring (Williams, 1983; Myers, 1985; Ng, 1988). ranges from Melbourne, Victoria, in the south The reason for the increased survival shown to Gladstone, Queensland, in the north and by many insects when feeding on more nutritious occurs both inland and ncar thc coast. food plants is generally unstated, but is prob- Populations are common but local (Common & ably related to the ability to increase growth Waterhouse, 1981). The field season is rates and hence reduce development time approximately November- April, in which (thcreby reducing mortality risk), to decrease time there may be up to three generations. feeding rates (thereby reducing mortality risk) Larvae feed on young plants of Acacia spp., and/or to the ability to invest more in defence and larvae and pupae are tended by mechanisms such as distasteful substances, tri- spp. ants. Adult females use ants chomes, etc., or immunological responses as cues in oviposition (Pierce & Elgar, 1985), to pathogens. The association of larvae of and usually lay eggs in crevices on the stems and Jalriierius evagoras (Donovan) with ants sug- branches of thc larval food plants. Sevcral egg gests a novel mechanism by which diet quality batches may be laid during one bout of may affect survival. oviposition. Caterpillars and pupae of J.evagoras secrete The field site where this rescarch was to ants an aqueous solution that has been shown performed was Mt Nebo, Queensland (152" to contain high concentrations of amino acids 47'E, 27" 23's). At sub-tropical Mt Nebo, (primarily serine) and sugars (Pierce, 1983, J.evagoras most commonly feeds on the hi- 1989). The tending ants have been shown to be pinnate A.irrorata (Sieb. ex. Spreng.) and is highly attracted to artificial solutions of those tended by ants of the I.~tic~p~species group (sp. amino acids found in the secretions. and the 25, Australian National Collection, attractiveness of pupae to ants has been cor- Canbcrra), hcreafter /.aizcep.s for short. related with the concentration of serine in The effect of fertilizer application to food washings (Pierce, 1083). Ants provide pro- plant or1 the attractiveriess of larvae to mils. One tection in return for the secretions (Pierce hundred potted food plants of A.dc,curreri.s et al., 1987; Baylis, 1989). This suggests that (Wendl.), grown from seed by the Department caterpillars feeding on more nutritious food of Forestry, Forbes, N.S.W., were rcported in a Ho.st-plarit effects oti ail ant-terided butterfly 3

mixture of 60% (by volume) vermiculite and The number of ants tending each was 40% clay soil from Mt Nebo. The plants were recorded daily for 10 days. Ants were defined as 66210 cm (mean ISD, 11 = 100) tall. 'tending' if they were in physical contact with a Plants were randomly assigned to one of two larva. To obtain an estimate of the inherent treatments: (a) From early February to April attractiveness of fertilized and unfertilized 1988 fertilized plants were watered every 2 days plants to ants, the number of ants on the plants with 200 ml water containing AquasolTM ferti- without larvae was also recorded. lizer (N:P:K ratio = 23:4:18) and chelated iron The effect of fertilizer application to food plant (both Hortico (Aust) Pty Ltd, Victoria), at oti the survival of larvae. In the arrangement concentrations of 0.8 g/l and 0.2 g/l respectively. described above, larval survival was measured Iron was added because this is often a limiting by scoring the number of larvae present on each element in Australian soils, and thus might plant (out of the original four or six) on each of prevent the uptake of additional nitrogen, the 10 days. (b) For the same time period, unfertilized plants To examine the direct effect of fertilizer appli- were watered every 2 days with 200 ml water. cation to the food plant on caterpillar survival, During especially hot periods, when there a control group of twelve plants was randomly was a risk of dehydration, all plants were given selected from the pool. These plants were set an additional 200 ml water on the intervening up without ant protection by banding their stems days. with tape, and completely coating the bands In early April 1988 all plants were examined with tanglefoot. Since caterpillars of ./.wagoras for the presence of root nodules. All of the cannot survive in the wild without ants (Pierce unfertilized plants, and none of the fertilized et al., 1987; Baylis, 1989), the plants were ran- plants, were found to have root nodules. This domly arranged in a bush house (a wooden is expected: nitrogen fixation is energetically construction lined with plastic mesh) which ex- costly and when an alternative source of nitro- cluded predators and parasites. The bush house gen is available (in this case, fertilizer) nodules was immediately adjacent to a natural tree are not maintained (Lie, 1974). bearing ant-tended /.evagoras and was within Experimerital method. Twenty-four food 10 ni of one of the experimental sites. plants from the pool of one hundred were ran- Final instar larvae were placed on the plants domly assigned to two experimental groups of as described above, and the number of surviving twelve, with equal numbers of fertilized and larvae was scored daily for 10 days. unfertilized plants in each group. At each of The effect of fertilizer application to larval two sites in paddocks around Mt Neb0 the food plant on the ovipositiorial hehuviour of groups of twelve plants were arrangcd in random /.evagorus. In late March 1988, four hundred order in a semicircle around a natural tree on pupae of J.evagoras were collected from trees which ants were tending larvae of J.evagoras. of A.binervata at Ebor, N.S.W. (150" 00' E, 30" The trees at the two sites were tended by differ- 34' S). Upon eclosion, adults were randomly ent colonies of 1.anceps. The stems of the potted allocated to five 1 m3 butterfly cages. The cages plants were banded with tape and the bands were wooden, with wire-mesh sides, and the half-coated with tanglefoot (Tanglefoot Co., wood was covered in aluminium foil to prevent Grand Rapids, Michigan). Ants were still able oviposition on the cage itself. The number of to climb the plants. Metal wire fences around in each cage ranged from thirty to the experimental sites prevented interference sixty during the experiment. Each day the but- from horses. terflies were provided with a 10% honey solution At the start of the experiment (day 0) fifth for food. instar caterpillars of J.evagoras were collected Four fertilized and four unfertilized plants from natural trees of A.irrorata around Mt were placed in each cage. The plants used were Nebo. Four individuals were placed on each of selected randomly from the pool described three fertilized and three unfertilized plants at earlier. The butterflies were allowed to mate both sites (hence twelve plants in total). On day and oviposit freely within each cage. After 4, two more caterpillars were placed on each of 5 days all plants were removed and the number the twelve plants. At each site, six plants were and size of egg batches laid on each plant was not given any caterpillars. scored. 4 M. Baylis and N. E. Pierce

Water and nitrogen content of leaf samples. Sample leaves (in each case the fourth leaf from the tip of the plant) were collected from the fertilized and unfertilized plants used in the experiments described above. Water content (per cent fresh weight) was determined by weighing fresh samples, drying to constant weight at 60°C and reweighing. Dried samples werc digested with the micro-Kjeldahl method (Allen et al., 1986) and analysed for total ni- trogen content with a Technicon AA2 auto- analyser at the Department of Zoology, Oxford. Nitrogen content of the bipinnate food plant, A.decurrens, was determined for the pinnules, and not the mid-ribs, since these are the leaf part eaten by larvae of J.evagoras. Statistical analysis. All analyses were based Fig. 1. Mean (+ SE) number of ants tending fifth on the methods of Sokal & Rohlf (1981). instar caterpillars of J.evugorus on host plants which did (solid columns), or did not (hatched columns), receive nitrogenous fertilizer. Results

Effect of fertilizer application on ant attendance 0.05). Larvae on unfertilized plants were The leaves of plants treated with fertilizer tended on average by five to six ants each, had a higher nitrogen content than the leaves of whereas those on fertilized plants were tended unfertilized plants, but there was no difference by seven to eight ants each. in water content of the leaves or height of the In the absence of caterpillars, fertilized plants plants (Table 1A). were not more attractive to ants than unfcrtn- Fifth instar caterpillars of J.evagoras feeding lized plants. There were six plants without on fertilized plants were tended by a significantly caterpillars at each site: a single ant was oh- larger number of ants than caterpillars feed- served on an unfertilized plant at site 1 on one ing on unfertilized plants (Fig. 1; two-way occasion; many ants were observed on an unfer- ANOVA of site and treatment on mean number tilized plant at site 2, but these were tending an of ants per larva per plant, Fl,s = 5.29, P = hornopteran.

Table 1. Height of plant, nitrogen content (YO dry weight) and water content ('% fresh weight) of fertilized and unfertilized host plants used for: (A) the ant attendance and caterpillar survivorship experiments; and (B) the oviposition experiment. Data were log transformed prior to analysis by unpaircd I-tcst. - Fertilized plants Unfertilizcd planls /-value

Mean SD N Mean SD N

A. Height (cm) 68.44 10.25 24 61.86 7.29 24 - 0.209 '% nitrogen 3.89 0.14 23 2.38 0.40 24 X.703*' '%" water 65.23 2.92 23 64.91 3.44 24 0.358 B. Height (cm) 73.86 9.11 20 69.15 11.00 20 1.51 YO nitrogen 4.76 0.63 20 2.96 0.s0 20 10.08*" %, water 69.31 3.42 20 62.99 2.42 20 6.72**

P.ro.(mOl. Host-pluri/ ejyects oti an ant-tended butterfly 5

Effect of fertilizer application on caterpillar Effect of fertilizer application on adult survival oviposition In the absence of ants, fertilizer application The leaves of plants treated with fertilizer had no effect on the survival of caterpillars over had a higher nitrogen and water content than the 10-day period (Fig. 2, control). On no the leaves of unfertilized plants, but there was occasion did the proportion surviving differ sig- no difference in height of the plants (Table 1B). nificantly between fertilized and unfertilized Females of J.evagoras oviposited a total of plants. 1659 eggs on fertilized plants and 274 eggs on When ants were present, caterpillars on fer- unfertilized plants. This difference could be tilized plants survived better than caterpillars achieved in three ways: ovipositing on a larger on unfertilized plants (Fig. 2, sites 1 and 2). The number of fertilized plants; laying more egg difference in proportion surviving was most batches on fertilized plants; or laying larger egg marked after 6 or 7 days (two-way ANOVA of batches on fertilized plants. treatment and site on proportion surviving per Females oviposited on a larger number of plant, data arc-sine square root transformed; fertilized than unfertilized plants although the clay 6, F,,x = 4.40, P<0.07; day 7, F,,x = 4.00, difference was not significant (Fig. 3; Fisher's P = 0.08). The proportion surviving did not method of combining probabilities, found differ between sites. It thus appears that the for each trial from the binomial expansion, enhanced ant attendance of larvae caused by x2 = 9.96, d.f. = 10, P < 0.1). Considering only the application of fertilizer to the host plant led those trials in which eggs were found on plants to increased survival of the larvae, although the of both treatments (trials 2, 4 and 5), sig- increase was not significant at P = 0.05. nificantly more egg masses were laid on fertilized At both the experimental and control sites plants than unfertilized plants (Fig. 3; Fisher's the overall survival was low. This may in part be method of combining probabilities, found for attributed to emigration. Transferring cater- each trial by Mann-Whitney U-test, x2 = 15.13, pillars from A .irrorata to the closely related d.f. = 6, P < 0.05). However, the mean number A.decurrens caused some to leave or fall off the of eggs within each of these egg batches did not plant soon after being placed on it. differ significantly (Table 2). The larger number

Control 7

I

1'1.1' 0 2 4 6 8 100 2 4 6 8 100 2 4 6 8 10 Day

Fig. 2. The cffcct of fertilizer application on the survival of larvae of J.evugorav at two sites where ants were allowed to tend, and one control site where ants wcrc excluded. Points are means (tSE) of the proportion of larvae surviving on three plants (sites 1 and 2) and six plants (control). On day 0, four larvae were placed on each plant, and two more addcd on day 4. Open squares = fcrtilized plants: closed diamonds = unfertilized plants. ti M. Baylis and N. E. Pierce

; "1 E 15 F

" Trial 1 Trlal 2 Trial 3 Trial 4 Trial 5

Fig. 3. The oviposition preferences of J.evagoras presented with fertilized (F) and unfertilizcd (U) host plants:. The number of blocks per column is the number of plants (out of four) oil which thc butterflies ovipositcd. Thc: size of each block represents the number of egg masses laid.

of eggs laid on fertilized plants is thus due to fertilized food plants are able to attract a larger females choosing these plants more frequently ant guard which thereby enables them to survivc for oviposition, rather than females laying sig- better. Female adults of J.evagoras prefer to nificantly larger egg batches on these plants. oviposit upon fertilized food plants. A possible cue used by females of J.evagoras to discriminate between the fertilized and un- The uttructivenem 01 larvae to urits fertilized plants was colour. The intensity of green colour of leaves from the plants was Larvae on fertilized plants were more attract- ranked on a scale from 1 to 7 by an independent ive to ants than larvae on unfertilized plants.. observer without knowledge of their fertilized The reason for this increased attractiveness is or unfertilized status. The leaves of fertilized unclear, but is probably related to two factors: plants were darker than those of unfertilized (a) The rate of secretion of larvae may have plants (Mann-Whitney U-test, P < 0.01). been higher on fertilized plants. To increase the rate of secretion would require the increased loss of both water and nutrients. Since the ferti- Discussion lized plants had higher nitrogen, but not higher water contents than the unfertilized plants, such The experiments described in this paper dem- increased water loss would probably have re- onstrate that larvae of J. evagoras feeding on sulted in lower fresh growth rates, unless there

Table 2. Mean size of egg batches laid on host plants which citlier were, or wcrc not, given nitrogenous fertilizer. Data were log transformed prior to analysis by two-way ANOVA. The effects of trial were removed from thc analysis.

Fertilized plants Unfertilized plants

Mean SD N Mean SD N

No. of eggs 21.2 34.1 44 22.8 15.4 12 FI,,,=O.XO ns Host-plant ejfect, on an ant-tended huttcvfiy 7 was dietary compensation. Growth rates were atornuriu was dependent on the nitrogen level not examined in this experiment. (b) The con- of the host plant (Ohmart et ul., 1985). At centration of nutrients in the secretion may nitrogen contents below 1%, increases in nitro- have been higher for larvae fecding on fertilized gen led to increased size. At nitrogen contents plants. Secretions were not analysed chemically, between 1% and 3%, increases in nitrogen and therefore it is not possible to specify which content had no effect on size. The unfertilized nutrients (if any) were of increased concentra- food plants of J.evagoras used here had nitrogen tion in the secretions of larvae feeding on ferti- contents of between 2% and 3%. lized plants. However, the fertilized plants had A second explanation is that the application significantly higher nitrogen contents than the of fertilizer may not have altered the level of unfertilized plants, and the secretions of larvae those chemical compounds related to survival. of J.evagoras have been shown to contain amino The application of ammonium sulphate to plants acids to which ants are highly attracted (Pierce, of the ragwort, Senecio jacobaea, reduced the 1983, 1989). An important role for the amino levels of threc amino acids but had no effect on acid serine is possible. There is a positive corre- the levels of the other thirteen examined lation between the concentration of aqueous (Wilcox & Crawley, 1988). We used a P:K:N solutions of serine and their attractiveness to fertilizer: caterpillars of fieris rape survived foraging ants, and a positive correlation between better on plants fertilized with ammonium sul- the concentration of serine in washings of pupae phate and ammonium nitrate, but application of J.evagoras and their attractiveness to ants of urea did not affect survival, and application (Pierce, 1983). Unfortunately, in the latter of a P:K:N fertilizer actually decreased survival experiment possible covariances of serine con- (Myers, 1985). centration with that of other nutrients (such as In contrast, in the presence of ants, cater- sugars, which are also highly attractive to ants) pillars of .I. evagorus survived better on fertilized were not investigated. plants, although the difference was not quite The two hypotheses discussed above can be significant. This suggests a novel mechanism by readily distinguished by collecting secretions which diet quality may effect survival. On ferti- from larvae feeding on fertilized/protein- lized plants, larvae of J.evugorus are able to coated plants and on unfertilized/untreated attract a larger ant guard which provides a plants, and finding the protein concentration, greater defence against predators and parasites or by observing the rate of secretion of larvae (Pierce et al., 1987; Baylis, 1989). If such a feeding on the different diets. process is common to myrrnecophilous lycae- nids, one would expect an intimate link between diet and myrmecophily in the family. This is, in The survival of caterpillars on fertilized plunts fact, the case. At the levels of species and Many studies have demonstrated that increase , myrniecophilous lycaenids tend to feed in the nitrogen content of host plant or diet in- on leguminous (nitrogen-fixing) plants, other creases larval survival (Myers & Post, 1981; nitrogen-fixing plants and on mistletoes (Pierce, Lincoln et al., 1985; Myers, 1985; Ohmart et al., 1985). Nitrogen-fixing plants are likely to have 1985; Cates et al., 1987; Johnson & Bentley, either higher nitrogen levels in their leaves 1988; Taylor, 1988), although this is not always (Akeson & Stahman, 1966, cited in Pierce, the case (Stark, 1965; Lincoln, 1985). In the 1985) or to exhibit less temporal variation absence of ants, larvae of 1.evagora.y did not in nitrogen content because they are less de- survive better on fertilized plants. There are pendent upon fluctuations in the nitrogen avail- several possible explanations. Firstly, the leg- ability in the soil. Similarly, as a result of their uminous food plants of J.evagora.7 may be suf- parasitic lifestyle, mistletoes may exhibit little ficiently rich in nitrogen that it is not a limiting temporal variation in nitrogen content (Urness, element in physiological processes: further in- 1969, cited in Pierce, 1985). The link between creases in nitrogen content may not stimulate myrmecophily and diet in lycaenids is demon- greater health and/or allow greater investment strated further by their predilection for nitrogen- in defence mechanisms. For example, the effect rich plant parts such as flowers, seeds and of changes in nitrogen content (induced by terminal foliage (Mattson, 1980; Robbins & fertilizer application) on the growth of Paropsis Aiello, 1982). 8 M. Buylis utiil N. E. Pierce

trees with ants (Pierce, 1983) and seem to use Ovipositiorial responses of butterflies of chemical cues at short distance: adults flying J. evugorus around a tree appear to tap it with their antennac Ovipositing females laid eggs on a greater (Pierce & Elgar, 1985). number of fertilized than unfertilized plants, and on fertilized plants laid a larger number of egg batches. Similarly, females laid a larger Acknowledgments nuniber of egg batches on plants containing the attendant ant, I.anceps, than on plants without We thank Tim Anderson, Andrew Berry, ants (Pierce & Elgar, 1985). In neither case did Roxanna Keen, Roger Kitching, David Nash, the butterflies lay more eggs per egg mass. This Ben Normark, Darren Quinn and Martin Taylor adjustment of number of egg masses laid, rather for help in . Susan Brownsworth, than the number of eggs within each mass, in Charmaine Lickliter, Graham Snell and Alan response to environmental cues may not be Skates generously gave us access to their land. common to all lycaenids. Atsatt (1981) found Angela Douglas, Alan Grafen, Mark Pagel, that caged females of amaryllis, when Jane Rees, Steve Simpson, Sir Richard South- presented with branches of food plant, ovi- wood and Pat Willmer provided useful advice posited on branches both with and without ants, with statistics and comments on the manuscript. but laid larger egg masses on branches with Nitrogen analyses were performed by, or with ants. the help of John Castle. M.B. was supported by The ability of ovipositing butterflies to select a NERC studentship; N.E.P. was supported by food plants most suitable for their offspring has grant number BSP-8705483 from the National been demonstrated by various other studies Science Foundation. (Ivcs, 1978; Jones & Ives, 1Y7Y; Rausher, 1981; Rausher & Papaj, 1983; Williams, 1983; Ng, 1988; and see discussions by Singer, 1984; Chew References & Robbins, 1Y84). Our study adds to those that have demonstrated ovipositional preferences Allen, S.E., Grimshaw, H.M. & Rowland, A.P. for nitrogen rich plants (Wolfson, 1980; Myers, (1086) Chemical analysis. Methods in Plunf 1985; Taylor & Forno, 1987). Such preferences Ecology, 2nd edii (ccl. by P. D. Moore and S. B. may not always occur. Cinnabar moths, Tyria Chapman), pp. 285-344. Blackwell Scientific Pub- jucohueae, presented with ragwort host plants, lications, Oxford. Senecio jucohuea, did not oviposit upon more Atsatt, P.R. (1981) Ant-dcpcndcnt food plant sclcc- fertilized than unfertilized plants or lay larger tion by the mistlctoc buttcrRy Ogyris arnurylli., egg batches on fertilized plants (Wilcox & (Lycacnidae). Oecologia (Berlin), 48, 60-63. Crawley, 1988). No mention is made of the Baylis, M. (1989) The rolc of nutrition in an ant-- number of egg batches per plant. Interestingly, lycacnid-host plant interaction. D.PhiI. thesis, the application of fertilizer did not increase the Oxford University. Chtcs, R.G., Hcndcrson, C.B. & Rcdak, R.A. (1987) total nitrogen content of the plants, and larvae Rcsponscs of thc western spruce budworm to of T.jucohaeue on fertilized plants actually grew varying lcvcls of nitrogcn and tcrpencs. Oecologiu less than those on unfertilizcd plants. (Berlin), 73, 312-316. The exact cues by which female J.evagorus Chew, F.S. & Robbins, R.K. (1984) Egg-laying iii detect physiological differences in larval food butterflies. Biology of Butterpies (cd. by R. I. plants were not investigated. The fertilized Vane-Wright and P. R. Ackcry), pp. 65-79. plants had a higher nitrogen and water content Academic Prcss, London. (Table IB) and darker colour than unfertilized Common, I.F.U. & Watcrhouse, D.F. (1981) Butter- plants, but the application of fertilizer is likely flies of' Australia, 2nd edn. Angus & Robertson. to have caused a large number of physiological Sydney. Ivcs, P.M. (1978) How discriminating arc cahbagc changes which were not measured, but which butterflies'? Australian Journal of Ecology, 3, may be used as cues by the butterflies. Pieris 261 -276. rupae probably use colour as a long-distance cue Johnson, N.D. & Bentlcy, B.L. (1988) Effects ol and watednutrient cues upon contact (Myers, dictary protein and lupine alkaloids on growth and 1985). J.evagoras may be similar. Females use survivorship of Spodoptera eridania. Journal of long-distance visual cues in the detection of Chemicul Ecology, 14, 13Y 1- 1403. Host-plant ej1ect.v on ail ant-tended butterfly 9

Jones, R.E. & Ives, P.M. (1979) Thc adaptivcness of Behavioural and Ecological Sociobiology, 21, searching and host selection behaviour in Pieris 237-248. rapae (L.). Australian Journal of Ecology, 4, Raushcr, M.D. (1981) Host plant selection by Battus 75-86. philenor butterflies: the roles of predation, nutrition Lie. T.A. (1974) Environmental effects on nodulation and plant chemistry. Ecological Monographs, 5, and symbiotic nitrogen fixation. The Biology of 1-20. Nitrogen Fixation (ed. by A. Ouispel), pp. Raushcr, M.D. & Papaj, D.R. (1983) Demographic 555-582. North Holland P.C., Amstcrdam. consequences of discrimination among conspecific .incoln, D.E. (1985) Host-plant protcin and phe- hostplants by Battus philenor butterflies. Ecology, nolic resin cffects on larval growth and survival of a 64, 1402-1410. butterfly. Journal of Chemical Ecology, 11, Robbins, R.K. & Aicllo, A. (1982) Foodplant and 1459-1467. oviposition records for Panamanian Lycaenidae and .incoln, D.E., Newton, T.S., Ehrlich, P.R. & Riodinidae. Journal of the Lepidopterist’s Society, Williams, K.S. (1982) Coevolution of the checker- 36, 65-75. spot buttcrfly Euphydryas chalcedona and its larval Scribcr, J.M. & Slansky, F., Jr (1981) The nutritional food plant Diplacus aurantiacus: larval rcsponse to ecology of immature insects. Annual Review of protein and leaf resin. Oecologia (Berlin), 52, Entomology, 26, 183-211. 216- 223. Simpson, S.J. & Simpson, C.L. (1990) The mech- Mattson, W.J. (1980) Herbivory in relation to plant anisms of nutritional compensation by phyto- nitrogen content. Annual Review of Ecology and phagous insects. In: Focus on Insect-Plant Systematics, 11, 119- 161. Relations, Volume 2 (cd. by E. A. Bcrnays). CRC McNeill, S. & Southwood, T.R.E. (1978) The role of Press, Boca Raton, Florida. nitrogen in the development of inscctlplant Singcr, M.C. (1984) Butterfly-host plant relation- rclationships. Biochemical Aspects of Plant and ships: host quality, adult choice and larval success. Coevolution (cd. by J. B. Harbornc), Biology of Butterflies (ed. by R. I. Vane Wright pp. 77-98. Academic Press, London. and P. R. Ackery), pp. 333-353. Academic Press, Myers, J.H. (1985) Effect of physiological condition London. of the host plant on thc ovipositional choice of the Sokal, R.R. & Rohlf, F.J. (1981) Biometry, 2nd edn. cabbage white butterfly, Pieris rapae. Journal of W. H. Freeman & Company, New York. Animal Ecology, 54, 193-204. Stark, R.W. (1965) Recent trends in forest ento- Myers, J.H. & Post, B.J. (1981) Plant nitrogcn and mology. Annual Review of Entomology, 10, fluctuations of insect populations: a test with 303-324. cinnabar moth-tansy ragwort systcm. Oecologia Taylor, M.F.J. (1988) Field measurement of the de- (Berlin), 48, 151-156. pendence of life history on plant nitrogen and Ng, D. (1988) A novel lcvcl of inlcraction in plan- temperature for a hcrbivorous moth. Journal of insect systems. Nature, 334, 611-613. Animal Ecology, 57, 873-891. Ohmart, C.P., Stewart, L.G. &Thomas, J.R. (1985) Taylor, M.F.J. (1989) Compensation for variable Effccts of food quality, particularly nitrogen con- dietary nitrogen by larvae of the salvinia moth. centrations, of Eucalyptus blakelyi foliage on thc Functional Ecology, 3, 407-416. growth of Paropsis atomaria larvae (Coleoptera: Taylor, M.F.J. & Forno, 1.W. (1987) Oviposition Chrysomelidac). Oecologia (Berlin), 65, 543-549. preferences of the salvinia moth Samea multi- Pierce, N.E. (1983) The ecology and evolution of plicalis Guenec (Lep., Pyralidae) in relation to host symbioscs between lycaenid butterflies and ants. plant quality and damage. Journal of Applied Ph.D. thesis, Harvard University. Entomology, 104, 73-78. Pierce, N.E. (1985) Lycaenid butterflies and ants: Wilcox, A. & Crawley, M.J. (1988) The effects of selection for nitrogen fixing and other protein rich host plant dcfoliation and fertilizer application on food plants. American Naturalist, 125, 888-895. larval growth and oviposition behaviour in cinnabar Picrce, N.E. (1989) Buttcrfly-ant mutualisms. moth. Oecologia, 76, 283-287. Towarak a More Exact Ecology (cd. by P. J. Grubb Williams, K.S. (1983) The coevolution of Euphydryas and J. Whittaker), pp. 299-324. Blackwell Scien- chalcedonu butterflies and their larval host plants. tific Publications, Oxford. Ill. Oviposition behavior and host plant quality. Picrce, N.E. & Elgar, M.A. (1985) The influence of Oecologia (Berlin), 56, 336-340. ants on host plant selection by Jalmenus evagoras, a Wolfson, J.L. (1980) Oviposition response of Pieris mymecophilous lycaenid butterfly. Behavioural rapae to environmentally induced variation in and Ecological Sociobiology, 16, 209-222. Brassica nigra. Entomologia Experimentalis et Pierce, N.E., Kitching, R.L., Buckley, R.C., Taylor, Applicata, 27, 223-232. M.F.J. & Benbow, K. (1987) The costs and benefits of cooperation for the Australian lycaenid buttcr- fly, Jalmenus evagoras and its attendant ants. Accepted 26 February 1990