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Oecologia1982 9 Springer-Veriag
Coevolution of Pierid Butterflies and Their Cruciferous Foodplants
V. Habitat Selection, Community Structure and Speciation
Steven P. Courtney* Department of Zoology, University of Durham, England
Summary. Early models of hostplant exploitation by phytophagous insects suffer from unwarranted assumptions and may not be generally applicable. Wordmodels of the co-evolutionary approach may assume unwarranted evolutionary stability in 'strategic' explanations, whilst mathematical models derived from earlier optimal-diet studies are unrealistic and unwieldy. A simple arithmetic model synthesises these two approaches, using the two parameters of foodplant suitability and availability. Hostplant use by the butterfly Anthocharis cardamines, previously thought to be maladaptively polyphagous, is shown to be optimal under prevailing conditions of short search time. The predictions of the model for hostplant use and community structure of butterflies and other phytophagous insects are tested and, in large part, corroborated. Monophagy and monophagic forms of oligophagy are shown to be favoured by: long adult lifespan; low search costs to females; search images (whether visual or olfactory) ; batch-laying of eggs; high differential in foodplant suitability.
The paradigm of insect-plant coevolution is well-established and used generally to explain the patterns of hostplant use by insects. However, despite the efforts of Levins and MacArthur (1969), Jaenike (1978) and others, the coevolutionary approach seems little wedded to the corpus of ecological thought, deriving from MacArthur, which uses analytical models, particularly in the study of diet width (Emlen 1966; Pulliam 1974). The two approaches were developed contemporaneously, particularly by Ehrlich and Raven (1965) and MacArthur and Pianka (1966), but have concentrated on different subject matterns; insect/plant coevolutionary studies have been largely concerned with the mechanics of allelochemical and other interactions, and the adaptations employed by insects to exploit defended resources. In this paper I analyse foodplant exploitation by the Pierinae butterfly Anthocharis cardamines (L.), and derive a model combining elements of both foodplant suitability and of search time. This model belongs to the general family of optimal diet models (Sih 1979) but, unlike most of these, is constructed in terms of individual fitness rather than some (arguably) fitness-related quality, such as energy. Thus this optimality based study refutes the argument of Lewontin (1977) that all such optimisation models make large assumptions concerning relation to fitness. Predictions made from the model appear generally supported and pro* Present Address: Department of Zoology, P.O. Box 147, University
of Liverpool, England
vide a framework on which to understand the diversity of foodplant exploitation strategies to be observed in butterflies and other phytophagous insects. Wiklund (1974a) characterised two forms of olioligophagy as practised by insects. In one form (the 'polyphagic type') an insect population uses all available hostplants of a narrow range of species, showing no preference for any one; in the other form (the 'monophagous type'), the insect uses only one hostplant species in any one population, although using many species over its whole geographical range. Examples of the two types are respectively the butterflies Artogeia rapae (L.) (Takata 1961) and Euphydryas editha Bois. (White and Singer 1974). Studies on other butterfly species of either type have emphasised the importance of the relative suitabilities of different foodplants for larval development, and of the availability and predictability of foodplants, in determining which strategy is adopted (Wiklund 1973, 1975; Chew 1975, 1977a; Wiklund and Ahrberg 1978; Rodman and Chew 1980). In the earlier papers of this series (Chew 1975, 1977a) it was shown that oviposition behaviour of Nearctic Pierinae agreed well with the suitability of hostplants for larval survival, females avoiding oviposition on poisonous Cruciferae, with the exception of Thalspi arvense L., which is a recent introduction and may be behaviourally indistinguishable from acceptable hostplants (Rodman and Chew 1980). However it was subsequently shown that one Palaearctic Pierinae member, A. cardamines, laid proportionately most eggs on the worst foodplants available to it (Hesperis matronalis L. and Barbarea wdgaris R.Br.) - exactly the reverse of the distribution predicted (Courtney 1981). Differences in eggloads upon cruciferous hostplants were shown to be caused by differences in foodplant apparency; those species which successfully kill A. cardamines larvae being larger or persisting longer and hence more easily perceived by females searching for oviposition sites (Courtney 1982). The causes underlying greater use of poor foodplants were thus established, but there remains yet the problem of diet width - why are species which kill larvae used at all? A. cardamines eggs laid upon the major hostplant Alliaria petiotata Bieb. have a chance of surviving to the adult stage some five to six times that of eggs laid upon H. rnatronalis. Since A. petiolata is an abundant crucifer, with most oviposition sites unexploited by A. cardamines, the 'polyphagous type' pattern of foodplant use by the butterfly requires explanation. Wiklund and Ahrberg (1978) have suggested that hostplant use by A. cardamines reflects unpredictability in foodplant abundance and in mortality associated with different host species. I now examine this and other hypotheses for populations of A. cardamines studied in Northern England. Primary data and details of study sites are given by Courtney (1980, in prep.).
102 Four hypotheses are suggested to explain the use of less suitable hostplants by A. cardamines." Hypothesis l : F e m a l e s are unable to distinguish different hostplant species. Hypothesis 2: Insufficient time has elapsed for evolution to produce discrimination. Hypothesis 3 : The apparent lack of selectivity is a strategy in time and/or space against resource unpredictability. Hypothesis 4: Females are in fact maximizing reproductive effort, laying eggs on poor hostplants as a consequence of time constraints.
Stanton (1979), in research on chemotactile stimulation and oviposition of legume-feeding Pieridae, emphasised the need to recognise physiological limitations to discrimination by female butterflies amongst foodplants. Polyphagy is unsurprising if food plants are indistinguishable from one another. However, in a number of different crucifer-feeding species, insects have been shown to distinguish between different glucosinolates, each crucifer species typically having a unique profile of these precursors of the primary defence chemicals, the mustard oils (Nair et al. 1973; Hicks 1974; Sehgal and Vjagir 1977; Nielsen 1978). Rodman and Chew (1980) have argued that Pierinae females are well able to distinguish between Cruciferae by such glucosinolate profiles, except for certain cases where different species share similar profiles. H. matronalis and B. vulgaris contain quite different glucosinolates to A. petiolata (Kjaer 1976). Additionally Salmon (in prep.) shows convincingly that larvae of two Pierinae species are well able to distinguish amongst Co. Durham Cruciferae by chemosensory means. Thus it seems reasonable to assume that discrimination by females does or could exist in A. cardamines if selection is favourable. Hypothesis l is not favoured on available evidence. Chew (1977a, b) showed that oviposition on inappropriate hostplants by Nearctic Pierinae was in part explainable by historical factors. She argued that Thlaspi arvense, which kills larvae of North American Artogeia napi (L.), and which is an introduced species, has not been present in the butterfly's environment long enough for avoidance behaviour to evolve. Maynard Smith (1978) has detailed other similar examples of 'evolutionary lag', such as the inappropriate clutch size of some seabirds (Nelson 1964). Of the two hostplants species poor for A. cardamines larval survival, one (H. matronalis) is an introduced species in Britain. The introduction is probably of long standing, and the hostplant has been known for A. cardamines since Newman (1869) recorded both H. matronalis and B. vulgaris amongst the four hostplants most commonly used. One specimen of A. cardamines taken in Co. Durham in the year 1855 was found to bear pollen of H. matronalis when examined microscopically; thus it seems that the butterfly and crucifer have co-existed in the study area for at least 125 insect generations, arguably long enough for avoidance behavior to evolve ((Jones 1977) has shown how foodplant location behavior of A. rapae has changed in populations derived from common stock in the 19th Century). On the continent of Europe, H. matronalis is native and has probably been in proximity with A. cardamines for millenia; in Italy, at least, the plant is regularly used as a host (C.J. Hill, pers. comm.). 'Evolutionary lag', Hypothesis 2, does not appear tenable. Several authors have argued that the 'polyphagous type' of oligophagy is practised by Pierinae as a response to the unpredictability of larval foodplants and related mortality factors in either space or time, or in both. A. rapae (Takata, 1961), A. napi
(Chew 1977a) and A. cardamines (Wiklund and Ahrberg 1978) are all held to adopt this strategy in order to overcome fluctuations in resource availability and suitability. Chew emphasised the importance of variation in foodplant species in space; this does not appear to be a satisfactory explanation for A. cardamines in northern England. In 30 populations on a transect spread across some 75 km distance of the northern Pennines, taking in several habitat types, A. cardamines was always associated with the foodplants A. petiolata or Cardamine pratensis L. (Table 1). These two foodplants are amongst the best available for larval survival (Courtney t981) and are those typically regarded as the hosts of the butterfly in both Britain and Sweden. Of 48 British correspondents, only one has recorded an A. cardamines population which does not feed on either of these species. A. cardamines females which oviposited only on these two crucivers would not therefore experience substantially less predictability of foodptant species in space. Foodplant unpredictability in time is also unlikely to favour polyphagic strategies in British A. cardamines. At one major study site, Durham, the number of available hostplants was counted annually for 1977 to 1980 (Table 2). It is seen that although some variance occurs, in the four years of study, A. petiolata dominated the crucifer community of the riverbank study site. However, in Sweden more dramatic variations in crucifer abundance may occur in early successional habitat (C. Wiklund, pers. comm.). Wiklund and Ahrberg (1978) have emphasised that unpredictability of some foodplant associated mortality (such as drowning on marsh species) will lead to selection against specialisation on single hostplant species. Present evidence from northern England suggests strongly that most differences in larval mortality on different hostplants are however predictable. Based on a study of the survival of 1,798 individuals in the wild, I have argued that most differences in mortality reflect differences in the quality of the Cruciferae themselves as larval food, with mechanical and chemical defences killing many larvae on H. matronalis and B. vulgaris (Courtney 1981). Similarly B. vulgaris is seen to be a poor foodplant for Anthocharis spp. not only in Co. Durham, but also in Sweden (C. Wiklund, pers. comm.) and the U.S.A. (Chew 1977b). In the long term, evolution against the use of such a consistently poor foodplant should have occurred. Females of A. napi and A. cardamines avoid ovipositing on Erysimum which contains cardenolides, allelochemicals which seem to kill 100% of larvae grazing on the plants of this genus (Chew 1977; Wiklund and Ahrberg 1978). Additional problems also occur with the hypothesis of Wiklund and Ahrberg, and other 'strategic' formulations, not least the difficulty of investigating long-term processes. A major objection is that in situations of at least short term predictability (as at Durham), 'polyphagous type' oligophagy will not be evolutionarily stable against invasion by monophagous strategists. Polymorphism for the different strategies would then be expected (since monophagy will always lead to higher fitness in predictable conditions); Chew (1977a) has shown that this does not occur in oligophagous Pierinae. The maintenance of a pure 'polyphagous type' strategy by the whole population may then require group selection scenarios under this model. One further problem with the use of strategic explanations is that they explain even results exactly contrary to those predicted, for instance in the study of Rausher (1979), and used a posteriori they cease to have any claim to testability. Hypothesis 3 is not corroborated by available evidence. The remaining hypothesis holds that the behaviour of femlaes, in ovipositing on foodplants as they are found, is adaptive when time in which to locate hosts is limited. This hypothesis suggests that polyphagic strategists will always be favoured and hence
103 Table I. The principal and subsidiary hostplants of A. cardamines at 30 study sites in the North of England. Details of study sites are given by Courtney (1980) Locality Hostplants Principal Chester-Ie-Street Finchale Brasside Durham Sands Durham Shincliffe Hall Field Station Cassop Vale Bear Park Langley Moor Croxdale Brancepeth Witton Park Witton-le-Wear Wolsingham A Wolsingham B Key: Ap Ap Cp Ap Ap Hm Ap Hm Cp Cp Cp Ap Cp Ap Cp Ap Hm Ap Hm Ca Cp Ap Subsidiary By Hm Bv Hm Br Bv Cp So Bo Bv Ap Ca Bv Bv Cp Hm Br Bv Br Bv Ap By Hm Rs Cp Ca Cp Co Hm Stanhope Darlington Winston Ovington Barnard Castle Egglestone Middleton Dent Bank Coldberry Wearhead Alston Tynehead Nenthead Langwathby Locality Hostplants Principal Ap Ap Ap Ca Ap Ap Ap Cp Hm Ap Cp Cp Cp Ca Cp Hm Ca Cp Cp Cp Subsidiary
Ap Ap Co No Ta No
Ap AUiariapetiolata Bo Brassicaoleracea Br Brassicarapa Bv Barbarea vulgaris
Cardamine amara Cardamine pratensis Cochlearia officinalis Hesperis matronalis
No Nasturtium officinale Rs Rorippa sylvestris So Sisymbrium officinale Ta Thlaspi alpestre
Table 2. The number of individuals of major cruciferous hostplant
species at Durham in the years 1977 to 1980. Counts were made to the nearest 10 (A. petiolata) or 5 (other species), on patches of riverbank 1977 1978 10,320 230 225 185 55 1979 3,100 115 75 85 80 1980 7,010 390 450" 70 290 a
Alliariapetiolata Hesperis matronalis Barbarea vulgaris Brassica rapa Sisymbrium officinale
4,350 195 235 410 45
a On newly fallow agricultural land in 1980
predicts a pure population of polyphagic type, unlike Hypothesis 3. The major mortality factor in a key-factor analysis of the Durham A. cardamines population is failure of females to lay all their eggs (Courtney in prep.). In 1977, the year in which fecundity was highest, only 15% of eggs were successfully laid. In comparison to this shortfall of eggs, foodplant associated mortality is small, and if the two selection pressures are in opposition, it is readily seen that selection for increased fecundity might outweigh that for increased specificity of foodplant choice. It is suggested that, at Durham, A. cardamines females which search only for the best foodplants will lay less eggs than those which are indiscriminate, and overall fitness of such females will be lower when fecundity differences exceed those of larval survival Put simplistically, females will often do better to lay eggs on bad plants, rather than leave those eggs unlaid. I now develop a simple model to show that these conditions hold at Durham. In Swedish populations females may search for 2 h or more without finding hosts (C. Wiklund, pets. comm.) and it is likely that this model is applicable to all A. cardamines populations.
The relationship between host specificity and searching time in phytophagous insects has been addressed by Levins and MacArthur (1969) and Jaenike (1978). However these models have certain assumptions unsuitable here; that of Levins and MacArthur assumes that insects are unable to distinguish alternative hosts as either 'good' or 'bad', and must use either one or all available diet items; additionally it assumes that monophagy is ancestral, when in Pierinae the converse is implied. Neither model is easily applicable to the case ofA cardamines, and a new, simpler model was derived, which may prove more generally applicable. Let there be N foodplants, with j strategies of exploiting them, each successive strategy adding the next most favourable foodplant to the diet of the herbivore. Let tj be the searching time taken to find one plant under each strategy. When all hostplants are equally abundant: tl = 2t2 = 3t3 = Nt~ Let T be the total time available to a searching female, expressed in units of tN, that is the number of oviposition sites to be found in this time under strategy N. The number of eggs laid by each strategist (Ej) is then
where x is the maximum number of eggs to be laid and a is the proportion of necessary time available.
and takes values from 0 to 1, any excess over 1 being ignored. Then the fitness of strategy j (Wj) is :
104 Table 3. The number of 'available' plants (hi) of four Cruciferae at Durham 1977 to 1979. Availability = Abundance x mean A. cardamines eggload relative to A. petiolata (from Conrtney 1981). The mean fecundity of females in each year is also given 1977 1978 777 10,320 563 2,484 14,144 8.9 1979 357 3,100 188 1,173 4,818 9.4
No. of Foodplants Used Fig. 1. Values of the fitness quotient, W, for strategists using one
50 T= Srnall _ _
T= Max _ _
B. rapa A. petiolata B. vulgaris H. matronalis
1,722 4,350 588 2, i06 8,766
2 fecundity 22.6
where fi is the fitness of an egg reared on the ith foodplant, relative to the most favourable hostplant, taking values from Oto 1 (f~= I). As a simple example: when two equally abundant hostplants are available, one giving 100% survival of larvae, the other 50%. N=2 tl=2t 2
to four hostplant species, when abundances of the hostplants are equal. When time available for oviposition (7) is greater than or equal to the time required to lay all eggs under strategy 1 (T= Max), the optimal strategy is to lay all eggs on the best host. Below this value of T, the fitness of strategists 1 to 3 decays until when T= 150 (T=Small above), all possible eggs are laid only by strategists of type 4. For smaller values of T (when no strategist lays all eggs) the relative fitness of different strategists remains constant
I I I I I I I
let x = 100 and T = 150 t 2 150 al - 100x2
Br Ap Bv Hm
150 a2 - 100 =i
1 2 3 4 1 2 3 Fig. 2. The relative fitness of different strategies of foodplant util-
isation, using results for A. cardamines at Durham 1977-1979 to set parameters of hostplant suitability and availability, search time and egg number. Upper right are indicated the diet widths of the hypothetical strategists
In this case the two strategies leave equal numbers of surviving offspring, and neither is favoured by selection. To model the situation of A. cardamines at Durham, four foodplants of varying availability and suitability were incorporated. The 'availability' of a crucifer species is determined partly by its abundance, and partly by apparency to females (Table 3). Values offi are taken from Courtney (1980, 1981) where Brassica rapa L., a very suitable but uncommon plant is designated species 1 ( f l = l ) , Apetiolata species2 (fa=0.66), B. vulgaris species 3 (f3=0.28) and H. matronalis species 4 (f4=0.18). Then in 1977 (from Table 3) 8766 t3 - 6 6 6 0 = 1.32 8766 t2 = 6 0 ~ = 1.44 8766 tl - 1722 = 5.09
t 3 = 1.32
t 2 = 1.39
t 1 = 13.50
x = 150 (from Courtney in prep.). Calculating Ej as before, W j = e i f i where e i is the proportion of Ej laid on the foodplant.
t4 = 1 = 1
Similarly in 1978 t4= 1 t 3 = 1.21 t 2 = 1.27 tl = 18.20
and in 1979
Putting biological reality onto these terms, f~ represents the relative fitness of individuals reared on different foodplant species (relative to the best hosplant) as measured in the field. The other parameters that must be measured are: 1. The relative abundance (ni) of each hostplant biased if necessary, as here, by the apparency of different species; 2. The realised mean fecundity of the insect population (which itself requires estimates of adult female and egg population sizes). Fecundity will then be equal to T in a polyphagous species. Egg and plant population levels are relatively easily determined, as are the relative suitabilities of hosts in many cases. Accurate determination of adult
105 Table 4. Values of the selection coefficient s on comparing strategies of foodptant exploitation, when T is set from fecundity at Durham 1977-1979 Selection For strategy 4 Against strategy 3 2 1 2 1 1 0.09 0.13 0.72 0.04 0.69 0.68 0.07 0.09 0.91 0.04 0.90 0.90 0.11 0.13 0.85 0.03 0.83 0.82 1977 1978 1979 Table 5. Observed correlations between species richness of Western Palaearctic butterfly genera and the proportions of those species which are habitat or foodplant specialists. Habitat and hostplant data largely from Higgins and Riley (1975). Genera with only one representative species, and migratory African (2) and American (1) species were excluded. Data were arcsine transformed before computation. The association between species richness and degree of habitat specialism is consistent when genera of each Family are examined separately. (Species were classed as generalists when they occurred in more than one habitat type or utilised foodplants from two or more genera). Correlation between Habitat specialism Foodplant specialism Foodplant specialism Species richness Species richness Habitat specialism n df r p
71 69 69
69 67 67
0.323 -0.023 -0.052
0.001 n.s. n.s.
population size is generally more difficult, but is satisfactory for northern English A. cardamines where little emigration occurs. Figures 1 and 2 present the results of calculating the relative fitness of the four strategies of using the available hostplants, given varying amounts of search time (T) (Fig. 1 is a general model, given equal host abundance. Figure 2 is based on the observed A. cardamines data.). In all cases, as the value of T decreases, strategies using most foodplants become progressively more favoured. The true value of T is known for Durham in the three years, since the mean number of oviposition sites found under strategy 4 is also the mean fecundity of the A. cardamines females, which varied from 8.9 to 22.6 eggs per female. In every year of study, conditions of foodplant availability and suitability strongly favour the polyphagous form of oligophagy. This is made particularly clear in Table 4, which presents the selection coefficients amongst different strategies. s=l fitness of less fit strategy fitness of more fit strategy"
It is seen that very large values of s are obtained, selection strongly favouring polyphagy in A. cardamines populations at Durham. Discussion Foodplant exploitation in A. cardamines may be shown to be adaptive in this model. It should equally be applicable to other analyses of foodplant use by insects, broadly predicting polyphagy or 'polyphagous type' oligophagy when differences in foodplant quality are small and time limitation prevails. When differences in host plant quality are very large, monophagic forms may however be favoured. Similarly when search costs are small, monophagy may arise. For instance tropical butterflies are typically iteroparous and may not suffer time shortage and egg shortfall as do temperate species. Hence tropical species should be more generally monophagous, and more selective of oviposition sites. Scriber (1973) described, but was then unable to explain, marked increases in foodplant specialism towards the Equator in Papilionidae. Another example where time costs are small occurs when a species lays its eggs in clusters. Here, a female has only to locate a very few hostplants, egg shortfall will again be small, and monophagy may be favoured. Some of the best known examples of monophagous species are indeed cluster layers. Aglais urticae lays egg batches only on nettles, Urtica dioiea, choosing plant patches of large size (pers. ob.); alternatively batchlayers may show the monophagic form of oligophagy, as Euphyd-
ryas editha, which typically lays clusters on only the best hostplant species in any one area (Singer 1971). Analogous situations may exist for other phytophagous insects; broadly, insects which have only to locate one or a few food-items (e.g. adult phytophagous beetles) should more often be monophagous than insects which must locate many hosts (e.g. ovipositing Lepidoptera). One interesting possibility is that searching female butterflies may decrease search costs by monophagy if they employ a search image to increase search efficiency. Known examples of search images are in Pap ilio machaon L. (Wiklund 1974b), oligophagous Heliconids (Gilbert 1975) and Battusphilenor L. (Rausher 1978). P. machaon and B. philenor do indeed show the monophagous form of oligophagy. Further interesting deductions may be made from the model, which bears some similarities to the seminal optimality model of MacArthur and Piauka (1966), for the special case when search time is long, but pursuit/handling time very short. That earlier model established that a predator/herbivore in a patchy environment should not specialise on food types, but rather on a habitat type, especially when several species of predator coexist. In the present case, it is to be expected that Pierinae and other butterflies should be isolated from interspecific competition more by habitat differences than by differences in hostplants. This contrasts with the word-model of Zwolfer (1974), who argued that phytophagous insects may often coexist by utilising different food resources, but agrees well with observations on butterfly community structure (Gilbert and Singer 1975). Petersen (1954) and Ohsaki (1979) showed that Pierinae butterflies appear to be separated ecologically more by habitat than foodplant choice. Similarly some Satyridae (Shapiro and Carde 1970) and Heliconidae (Benson 1978; Young 1978) appear to partition environments by habitat selection. It should be noted that using the same resources in different ways also meets the requirements of the models - for instance the siliqua and leaffeeding guilds of Pierinae avoid competition by using different plant parts. Changes in habitat selection do occur in butterflies. British populations of Papilio machaon and northern populations of A. cardamines both exhibit narrowed habitat range, as do some E. editha populations (Gilbert and Singer 1975). Hence it may be that at low taxonomic levels, habitat shifts are more frequent than foodplant shifts. Species richness in western Palaearctic butterflies is indeed related not to foodplant specificity but to habitat specificity (Table 5). Either causal relationship is possible
species rich genera may have to partition their environment; alternatively habitat specialism may encourage diversification, isolation and hence speciation (for instance mountaintop specialists often speciate from lowland relatives). This is a mild departure from the orthodox coevolutionary viewpoint of Ehrlich and Raven (1965) where taxonomic divergence was associated primarily with foodplant shifts; however there is no conflict since I am here concerned with lower, basically infra-specific levels of organisation. The model does not, on the face of things, appear to favour the evolution of monophagous Pierinae. By far the majority of studied species do indeed adopt the 'polyphagous' form of oligophagy viz. Artogeia rapae L., A. napi L., A. melete Men., Pontia dapIidice L., P. sisymbrii, Euchloe ausonia Hbnr and related species, E. belemia, E. tagis Hbnr, E. olympia Edw., Anthocharis lanceolata Bois. and A. sara Bois. Two species previously thought monophagous, Zegris eupheme Led. and Anthocharis belia, use several Cruciferae in Morocco, and conform to this type also. There yet remain some species which are however monophagous, viz. Artogeia bryoniae 0., A. virginiensis Edw., A. ergane Gyr. (all taxonomically close to the 'polyphagous type' A napi) and A. krueperi Stgr. (close to A. rapae). All these four are also habitat specialists, A. virginiensis specialising on shaded woodland (Hovanitz 1963), the other species on mountainous habitats. In all cases, the range of hostplants available is severely limited. A. bryoniae is associated with the crucifer genus Biseutella, but will use other hostplants, such as H. matronalis, when these are introduced into its habitat (Varga 1965). A. virginensis is similarly facultatively monophagous upon Dentaria diphylla Michx. (Bowden 1970). In these two species (and possibly in A. krueperi) it is seen that habitat specialism has led to facultative monophagy and as a result of this further adaptation may ensue. A. virginiensis is for instance univoltine, a derived characteristic from bivoltine ancestors - an adaptation to vernal growth of Dentaria (Shapiro 1971). Smiley (1978) has outlined how ecological factors may cause such progressive specialisation in some tropical butterfly species, even when foodplants are abundant. In the case of A. ergane, such progressive specialisation on an available resource, through facultative monophagy, has lead to a truly obligate monophagic relationship with the crucifer Aethionema saxatile L. (Lorkovic 1968), where the larvae have abandoned the normal Pierinae ground colour of green to camouflage themselves on the blueish leaved crucifer. Thus, even in populations where time constraints operate, monophagic relationships may evolve, if few host species are available. The model described above is simple, testable, and easily modified to take account of potential variables. At present monophagy or the monophagous form of oligophagy is predicted in butterflies only from the following situations: extreme differences in foodplant suitability; low search costs, whether due to long adult lifespan, batch laying or the possession of a search image; hostplant isolation in time or space.
Acknowledgements. This research was carried out during the tenure
of a research studentship of the S.R.C., and was supervised by Lewis Davies to whom I am especially grateful. RR. Baker, S.R. Bowden, F.S. Chew, Sarah Courtney, J.P. Dempster, P. Dugan, T. Dunn, C.J. Hill, and colleagues at the Universities of Durham and Liverpool have all made useful comments. I owe a special debt to Christer Wiklund, for much discussion and encouragement.
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