Patch marking in the aphid hyperparasitoid,Dendrocerus carpenteri: the information contained in patch marks

The aim of this study was to test if females of the aphid hyperparasitoid Dendrocerus carpenteri (Curtis produce patch marks. We tested if these marks inform a foraging female of the identity of the producer of the mark (the female herself or a conspecific female) and on the producer's success or failure in finding hosts in the marked area. We also tested if the responses to patch marks differ depending on the size and/or egg load of the female. On average, females walked shorter paths and spent less time in previously explored areas in comparison to control areas only if the area had first been explored successfully (host found) by a conspecific female. If no host had been found or if the area had been explored by the same female previously, no differences between average values were recoreded. However, egg load also seemed to influence foraging decisions in those experiments where average values were not different between previously explored and control areas. Females with a low egg load tended to spend less time in previously explored areas than females with a high egg load. Average values therefore somehow obscured the individual responses to pathc marks. The results suggest that at least D. carpenteri females with a low egg load continuously apply a marking pheromone while walking. This pheromone seems to contain information on the identity of the producer. In addition, different pheromones seem to be applied depending on whether or not hosts are present in the area.     

Nocturnal activity and resource utilization in the aphid hyperparasitoid, Dendrocerus carpenteri

Abstract.

• 1 Females of the aphid hyperparasitoid Dendrocerus carpenteri (Curtis) search successfully for hosts during both day and night. Oviposition numbers per host patch did not differ significantly between day and night.
• 2 D.carpenteri females also displayed a nocturnal flight activity, showing that they are not only capable of searching on a given host plant but also of dispersing between host plants.
• 3 Nocturnal oviposition activity was mainly influenced by egg load. Females with a high egg load laid more eggs at night than females with a comparatively low egg load. Thus, D.carpenteri females may use nocturnal foraging to compensate for the lack of oviposition opportunities during day.
• 4 D.carpenteri females which foraged continuously for hosts both day and night (= for 24 h per day) benefitted from an 1.4-fold increase in lifetime reproductive success when compared to females which foraged only by day (= for 16 h per day).
• 5 The benefit of night foraging for this species is a significantly increased reproductive success.

     

Sex-ratio bias in an aphid parasitoid-hyperparasitoid association: a test of two hypotheses

Abstract.

• 1 We tested the hypothesis that biased sex ratios in the aphidiid parasitoid, Aphidius ervi, are the result of sex-specific mortality of immatures due to hyperparasitism. The solitary hyperparasitoid, Dendrocerus carpenteri, deposits its eggs on the prepupa or pupa of the primary parasitoid after its pea-aphid host is mummified.
• 2 In dichotomous choice tests, females of D.carpenteri accepted immatures of both sexes of A.ervi with equal frequency. Independent of the sex of the primary parasitoid, the probability of a mummified pea aphid being hyperparasitized did not differ between large (adult at the time of death) and small (fourth nymphal instar) mummies.
• 3 As predicted by‘host quality’models of offspring sex allocation, D.carpenteri produced a higher proportion of female than male offspring in large mummies. These laboratory results were supported by field data.
• 4 Because hyperparasitism by D.carpenteri is random with regard to host sex, it should have no influence on optimal sex allocation by the primary parasitoid.

     

Influence of host distribution on foraging behaviour in the hyperparasitoid wasp, Dendrocerus carpenteri

The foraging behaviour of Dendrocerus carpenteriCurtis (Hymenoptera: Megaspilidae), an ectophagous hyperparasitoid of aphidiine wasps inside mummified aphids, was examined in the laboratory with an experimental system consisting of broad bean, Vicia fabaL, the pea aphid, Acyrthosiphon pisumHarris, and a primary parasitoid, Ephedrus californicusBaker. Pea aphids parasitised by E. californicusoften disperse from their feeding sites (or off host plants) before dying and mummifying. Response of female hyperparasitoids to host distribution was evaluated at two spatial scales. At the first scale, behaviour of hyperparasitoids was examined on individual plants with different densities of hosts. At the second scale, habitat complexity and host location were manipulated in large foraging cages containing several plants. I show that patterns of density-dependent hyperparasitism can result from the foraging behaviour of D. carpenteri. However, dispersal of parasitised aphids may not reduce the incidence of hyperparasitism if hyperparasitoids systematically search the habitat.     

Host selection and larval interactions among three primary parasitoids ofPlathypena scabra (Lep.: noctuidae)

Three hymenopteran parasitoids that attackPlathypena scabra (F.) larvae often oviposit into consecutive instars of the host. We investigated host discrimination by adults and competitive interactions among larvae of these three parasitoid species. Avoidance of superparasitism byCotesia marginiventris (Cresson) andDiolcogaster facetosa Ashmead was tested. Females of each species were presented either withP. scabra parasitized by a different female of the same species 6 h earlier or unparasitizedP. scabra. Under these conditions,C. marginiventris attacked similar numbers of parasitized and unparasitized hosts.D. facetosa attacked 31% fewer parasitized than unparasitizedP. scabra. The avoidance of multiple parasitism byD. facetosa was studied in a similar bioassay. AlthoughD. facetosa females parasitized fewerP. scabra that had been attacked byC. marginiventris 6 h previously, the reduction in parasitism was only about 23%. In competition studies, immatureD. facetosa were better competitors than immatureC. marginiventris. Aleiodes (=Rogas) nolophanae (Ashmead) was an inferior competitor against bothC. marginiventris andD. facetosa when the duration between parasitism events was 1 h, but their competitive ability increased when they multiply parasitized hosts at least 32 h after the initial oviposition.     

Intra- and interspecific competition by Fopius arisanus and Diachasmimorpha tryoni (Hymenoptera: Braconidae), parasitoids of tephritid fruit flies

Fopius arisanus (Sonan) and Diachasmimorpha tryoni (Cameron) are two important solitary endoparasitoids of tephritid fruit flies. The former species attacks host eggs while the latter attacks host larvae, and both species emerge as adults from the host puparium. This study investigated intrinsic competition between these two parasitoids, as well as aspects of intraspecific competition within each species in the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Parasitization by F. arisanus resulted in direct mortality of host eggs and prolonged development of host eggs and larvae. Superparasitism by F. arisanus was uncommon when mean parasitism per host patch was <50%, but increased with rising rates of parasitism. Superparasitism by D. tryoni was more common. In superparasitized hosts, supernumerary individuals of F. arisanus were killed through physiological suppression, while supernumerary larvae of D. tryoni were killed mainly through physical attack. In multiparasitized hosts, dissections showed that 81.6% of D. tryoni eggs in the presence of F. arisanus larvae died within 3 days, indicating physiological inhibition of egg hatch. Rearing results further showed that F. arisanus won almost all competitions against D. tryoni. The ratio of D. tryoni stings to ovipositions was lower in hosts not previously parasitized by F. arisanus than in parasitized hosts, suggesting that D. tryoni can discriminate against parasitized hosts. The mechanism that F. arisanus employs to eliminate D. tryoni is similar to that it uses against all other larval fruit fly parasitoids so far reported. The results are discussed in relation to the competitive superiority of early acting species in fruit fly parasitoids, and to a possible competitive-mediated mechanism underlying host shift by D. tryoni to attack non-target flies following the successful introduction of F. arisanus in Hawaii.     

Differential Parasitism of Native and Introduced Snails: Replacement of a Parasite Fauna

The role of parasites in a marine invasion was assessed by first examining regional patterns of trematode parasitism in the introduced Japanese mud snail, Batillaria cumingi (= B. attramentaria), in nearly all of its introduced range along the Pacific Coast of North America. Only one parasite species, which was itself a non-native species, Cercaria batillariae was recovered. Its prevalence ranged from 3 to 86%. Trematode diversity and prevalence in B. cumingi and a native sympatric mud snail, Cerithidea californica, were also compared in Bolinas Lagoon, California. Prevalence of larval trematodes infecting snails as first intermediate hosts was not significantly different (14% in B. cumingi vs 15% in C. californica). However, while the non-native snail was parasitized only by one introduced trematode species, the native snail was parasitized by 10 native trematode species. Furthermore, only the native, C. californica, was infected as a second intermediate host, by Acanthoparyphium spinulosum(78% prevalence). Given the high host specificity of trematodes for first intermediate hosts, in marshes where B. cumingi is competitively excluding C. californica, 10 or more native trematodes will also become locally extinct.     

闭弯尾姬蜂与菜蛾盘绒茧蜂寄生菜蛾幼虫时的种间竞争

在室内25℃下,以菜蛾3龄初幼虫作寄主,研究了菜蛾盘绒茧蜂Cotesia plutellae和半闭弯尾姬蜂Diadegma semiclausum的种间竞争。当寄主供2种蜂同时产卵寄生时,2种蜂各自的寄生率与其单独寄生时无显著差异,合计寄生率比一种蜂单独存在时有所提高,但差异不显著。2种蜂均能产卵寄生已被另一种蜂寄生了的寄主幼虫。当寄主被2种蜂寄生的间隔时间很短（少于10 h）时,所育出的蜂绝大部分（80%以上）为绒茧蜂;当寄主先被绒茧蜂寄生,并饲养2天以上再供弯尾姬蜂寄生时,所育出的全为绒茧蜂;当寄主先被弯尾姬蜂寄生,并饲养2天以上再供绒茧蜂寄生时,寄主幼虫绝大部分不能存活,只有少部分能育出寄生蜂,且多为弯尾姬蜂。当2种蜂的幼虫存在于同一寄主体内时,2种蜂的发育均受到另一种蜂的抑制;绒茧蜂1龄幼虫具有物理攻击能力,能将弯尾姬蜂卵或幼虫致死。这些结果表明,菜蛾盘绒茧蜂与半闭弯尾姬蜂在同一寄主中发育时,前者具有明显的竞争优势。     

Patch Time Allocation by the Parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). III. Effects of Kairomone Sources and Previous Parasitism

We investigated the effects of kairomone sources and previous parasitism on the patch-leaving behavior of Diadegma semiclausum, a solitary endoparasitoid of larval Plutella xylostella. Individual female wasps were released onto an experimental plant, and were allowed to freely leave for an alternative host plant placed upwind of the experimental plant in a wind tunnel. In one experiment, the experimental plant was either intact, contained host damage alone, or contained both hosts and host damage. In another experiment, the plant was infested with either unparasitized hosts, hosts parasitized previously by the female herself, or parasitized by Cotesia plutellae, another larval endoparasitoid of P. xylostella. We analyzed the influence of kairomone sources, host types, and within-patch foraging experience on the patch-leaving tendency of D. semiclausum by means of the proportional hazards model. Presence of host damage, and unsuccessful host encounters as a result of host defenses decreased the parasitoids' patch-leaving tendency, while successful oviposition, self-superparasitism, and rejection of parasitized hosts increased their patch-leaving tendency. A conceptual model of the parasitoid's patch-leaving behavior is proposed on the basis of the results of current and previous studies.     

Recognition of heterospecific parasitism: Competition between Aphidiid (Aphidius ervi) and Aphelinid (Aphelinus asychis) parasitoids of Aphids (Hymenoptera: Aphidiidae; Aphelinidae)

The solitary parasitoids Aphidius erviHaliday (Hymenoptera: Aphidiidae) and Aphelinus asychisWalker (Hymenoptera: Aphelinidae) attacked but generally did not oviposit in pea aphids parasitized by the other species. Wasps selectively oviposited in unparasitized hosts when given a choice. Host discrimination depended on the recognition of internal cues. Females of A. asychiseither could not recognize or ignored A. ervi'sexternal host marking pheromone. Under most conditions, A. ervisurvived in superparasitized hosts, killing competing A. asychislarvae by physical attack and possibly physiological suppression. The outcome of larval competition was not affected by oviposition sequence or age difference between larvae; A. asychissurvived only when it had substantially completed larval development before the host was superparasitized by A. ervi.It is suggested that competition for host resources incurs a cost, for the winner in terms of reduced size or increased development time and for the loser in terms of lost progeny and searching time. Consequently, heterospecific host discrimination can be functional. Internal, and probably general, cues enable wasps to recognize and avoid oviposition in hosts already parasitized by an unrelated species.     

Interaction of a host plant and its holoparasite: effects of previous selection by the parasite

If parasites decrease the fitness of their hosts one could expect selection for host traits (e.g. resistance and tolerance) that decrease the negative effects of parasitic infection. To study selection caused by parasitism, we used a novel study system: we grew host plants (Urtica dioica) that originated from previously parasitized and unparasitized natural populations (four of each) with or without a holoparasitic plant (Cuscuta europaea). Infectivity of the parasite (i.e. qualitative resistance of the host) did not differ between the two host types. Parasites grown with hosts from parasitized populations had lower performance than parasites grown with hosts from unparasitized populations, indicating host resistance in terms of parasite’s performance (i.e. quantitative resistance). However, our results suggest that the tolerance of parasitic infection was lower in hosts from parasitized populations compared with hosts from unparasitized populations as indicated by the lower above‐ground vegetative biomass of the infected host plants from previously parasitized populations.     

拟寄生蜂的寄主标记研究进展

拟寄生蜂常借助寄主标记信息素 (host marking pheromone, HMP) 来辨别已寄生寄主和健康寄主,避免过寄生和多寄生,减少后代的种内和种间竞争。寄主标记有外部标记、内部标记和“容器”及区域标记3种方式。HMP来源于拟寄生蜂的杜氏腺、毒腺、输卵管、卵巢、卵或咽侧体,由触角或产卵器感受。目前已鉴定出几种拟寄生蜂的HMP,多数为饱和与不饱和烃类的混合物,但卡氏盾痣细蜂Dendrocerus carpenteri的HMP是保幼激素。拟寄生蜂对寄主标记的反应受HMP持效期,拟寄生蜂内部状况如载卵量、年龄、经验和学习,及外部条件如拟寄生蜂和健康寄主种群密度以及寄主种类的影响。本文还讨论了HMP研究的理论和实际意义。     

Host handling and specificity of the hyperparasitoid wasp, Dendrocerus carpenteri (Curtis) (Hym., Megaspilidae): importance of host age and species

The oviposition behaviour of Dendrocerus carpenteri (Curtis), an ectophagous hyperparasitoid of aphidiine wasps inside mummified aphids was examined. Hyperparasitoids were provided in the laboratory with pea aphids ( Acyrthosiphon pisum ) which had been parasitized by three different species of aphidiine wasps ( Aphidius ervi, Ephedrus californicus and Praon pequodorum ) ranging in physiological age from the late larval stage to the late pupal stage. Females accepted only the hosts inside mummified aphids; they ignored live aphids, and did not accept dead, but not yet mummified aphids, although the latter were sometimes probed with the ovipositor. Female behaviour in handling A. ervi or E. californicus mummies did not change with experience; handling and oviposition times were stereotypic. However, naive females needed experience to locate the cocoon of P. pequodorum and distinguish it from the empty aphid mummy. Host acceptance and specificity were influenced more by the developmental stage than the species of the primary parasitoid. In dichotomous choice tests, hyperparasitoids 'preferred' prepupae over younger pupae of A. ervi , but they did not distinguish between these stages of E. californicus; older pupae were accepted at a low rate. Host preference was not influenced by conditioning on the rearing host. We consider several constraints on the host range of D. carpenteri , and discuss alternative explanations of differential hyperparasitism in the field.     

The developmental strategy of an idiobiont ectoparasitoid, Dendrocerus carpenteri : influence of variations in host quality on offspring growth and fitness

Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae) is a solitary hyperparasitoid, which attacks prepupal and pupal stages of hymenopteran parasitoids inside mummified aphids. The larva feeds externally on the host, which is envenomed by the female at oviposition. To evaluate the influence of variations in host quality on the growth, development and fitness of D. carpenteri, we varied the size and developmental stage of the primary parasitoid host (Aphidius ervi Haliday), which was reared on different instars of pea aphid [Acyrthosiphon pisum (Harris)] and English grain aphid [Sitobion avenae (F.)]. Within each kind of host, females eclosed from the relatively larger mummies, while males eclosed from the smaller mummies. Host size and hyperparasitoid size were correlated, and females were larger than males. In hyperparasitoids developing on prepupal and pupal hosts, development time from oviposition to adult eclosion was proportional to size; females required more time for development than males. The mean relative growth rate was the same in males and females and increased with host quality, as predicted by the growth model of Mackauer and Sequeira (1993) for idiobiont parasitoids. Larvae developing on late-pupal stages and pharate adults of A. ervi were unable to consume sclerotized host tissues; they were smaller and needed more time for development. The average number of mature eggs at eclosion was six, except in females developing on suboptimal hosts, which contained only one egg or none. Egg volume was correlated with female size, possibly reflecting differences in larval ontogeny. We provide equations describing the relationship between host quality as indexed by hind-tibia length of the mummified aphid and adult body size in terms of dry mass, development time and mean relative growth rate of D. carpenteri. We discuss the usefulness of host size as a proxy of host quality for idiobiont parasitoids, and provide examples of exceptions. Received: 14 December 1997 / Accepted: 23 July 1998     

Evidence for a marking pheromone in host discrimination byCephalonomia Stephanoderis (Hym.: Bethylidae)

The bethylidCephalonomia stephanoderis Betrem is an ectoparasitoid that prefers to oviposit on the prepupae and pupae of the coffe berry borerHypothenemus hampei (Ferrari) (Coleoptera: Scolytidae). It has the ability to distinguish unparasitized from parasitized hosts and rarely lays more than one egg per host. The mechanism of this host discrimination byC. stephanoderis was investigated under laboratory conditions. For this, parasitoid eggs that had been deposited on host pupae were removed and pupae were then offered (individually and collectively) to individual female wasps. A total of 92% of individually offered hosts and 93% of collectively offered hosts were not parasitized. It is concluded thatC. stephanoderis recognizes a marking pheromone deposited into or onto the host, preceding, during, or after oviposition which enables female parasitoids to avoid self and conspecific superparasitism.     

Interspecific Relations Between Two Sympatric Species of Hymenoptera, Dinarmus basalis (Rond) and Eupelmus vuilleti (Crw), Ectoparasitoids of the Bruchid Callosobruchus maculatus (F)

Dinarmus basalis (Rond) and Epelmus vuilleti (Crw) are two Hymenopteran species, which are solitary ectoparasitoids of bruchid larvae. In the presence of seeds of Vigna unguiculata (Walp) containing hosts parasitized by E. vuilleti, a high percentage of D. basalis females avoided multiparasitism whatever the age of the eggs or the larvae present on the host. The least avoidance was observed when the hosts were parasitized by E. vuilleti 30 min beforehand. This avoidance behavior is adaptive and is related to the low survival chances of the D. basalis larvae when they are in interspecific competition with E. vuilleti larvae. The analysis of the behavior of D. basalis demonstrated that the avoidance of multiparasitism could be due to the perception of two signals; an external signal deposited on the surface of the seeds during the E. vuilleti oviposition phase and an internal signal due to the presence of the eggs and larvae at the surface of the hosts. E. vuilleti females did not avoid multiparasitism and multiparasitized the hosts bearing D. basalis eggs or larvae. The behavior of E. vuilleti females was not disturbed by the presence of its competitor. Under these conditions of interspecific competition, the survival chances of E. vuilleti larvae were very high whatever the age of its competitor D. basalis. The two species of parasitoids could move in a column containing healthy seeds of V. unguiculata and patches with seeds containing parasitized or unparasitized larvae. The distribution of D. basalis females introduced into these columns depended on the host quality. They avoided the patches containing the hosts parasitized E. vuilleti and were found in the patches with healthy hosts. The behavior of E. vuilleti females was very different; the distribution of the females and the parasitism and multiparasitism rates were not affected by the quality of the hosts present in the patches. The adaptive significance of the behaviors of these two species was analyzed in relation to the survival chances of their offspring.     

Host selection by the heteronomous hyperparasitoid Encarsia pergandiella: multiple-choice tests using Bemisia argentifolii as primary host

The ovipositional patterns of the heteronomous hyperparasitoid Encarsia pergandiella Howard (Hymenoptera: Aphelinidae) in the presence of its primary host Bemisia argentifolii Bellows & Perring (Hemiptera: Aleyrodidae), and in the presence or absence of conspecific and heterospecific secondary hosts (Encarsia formosa Gahan andEretmocerus mundus Mercet; Hymenoptera: Aphelinidae) were examined to assess host species preferences. Host preferences by heteronomous hyperparasitoids may affect the relative abundance of co-occurring parasitoid species and may influence host population suppression by the parasitoid community. Four combinations of hosts were tested: (1) B. argentifolii, E. mundus, and E. formosa, (2) B. argentifolii, E. formosa, and E. pergandiella, (3) B. argentifolii, E. mundus, and E. pergandiella, and, (4) B. argentifolii, E. mundus, E. formosa, and E. pergandiella. Arrays of hosts (24) were constructed in Petri dishes using leaf disks, each bearing one host. Thirty arrays of each host combination were exposed to single females for 6 h. All hosts were dissected to determine number of eggs per host. Encarsia pergandiella parasitized E. formosa hosts as frequently as E. mundus hosts. However, E. pergandiella parasitized either of these heterospecific hosts more frequently than conspecific hosts in treatments including two secondary host species. When a third parasitoid species was included in host arrays, E. pergandiella parasitized conspecific hosts as frequently as heterospecific hosts. Developmental stage of the hosts did not significantly influence host species selection by E. pergandiella. Our results indicate that host selection and oviposition by heteronomous hyperparasitoids like E. pergandiella, vary with the composition of hosts available for parasitization, and suggest a preference for heterospecific over conspecific secondary hosts.     

Foraging for mates in the hyperparasitic wasp, Dendrocerus carpenteri: impact of unfavourable weather conditions and parasitoid age

Males of the aphid hyperparasitoid Dendrocerus carpenteri (Curtis) were attracted by a sex pheromone released by conspecific females. The intensity of this cue, and thus female attractiveness, depended both on the female's mating status and her age. Only virgin females younger than 2 h were consistently recognized as mates by foraging males. Male age did not influence foraging and mating success. Empty mummies, from which females had emerged within the previous 10 min were attractive to males and examined intensively. Rain reduced the searching success of males, although the host plant Vicia faba provided sheltered places. Wind did not reduce mating success but prevented both sexes from leaving the host plant. Since the time of female attractiveness seems to be very limited, wind may have an enormous effect on the mating success of D. carpenteri in the field and thus on the population dynamics of this species. Received: 5 October 1998 / Accepted: 16 December 1998     

The Bionomics ofCoptera Haywardi(Ogloblin) (Hymenoptera: Diapriidae) and Other Pupal Parasitoids of Tephritid Fruit Flies (Diptera)

The endoparasitoidCoptera haywardi(Ogloblin) (Diapriidae) was discovered in Mexico attacking the pupae of the Mexican fruit fly,Anastrepha ludens(Loew). Typically, parasitoids of Diptera Cychlorrhapha pupae develop as ectoparasitoids and are generalists that attack hosts in a number of families. Aspects of the bionomics ofC. haywardiwere compared to those of two chalcidoid ectoparasitoids,Dirhinus himalayanusWestwood andSpalangia geminaBoucek.C. haywardideveloped in three genera of Tephritidae, but not in species of other families. The two species of chalcidoids developed in all the calypterate and acalypterate hosts to which they were exposed. In an olfactometerC. haywardipreferredAnastrepha suspensa(Loew) pupae, while the chalcidoids preferred the pupae ofMusca domestica L.This preference inS. geminawas diminished in insects that had been reared onA. suspensa. C. haywardioviposited in theA. suspensapupae that had been previously parasitized by the braconidDiachasmimorpha longicaudata(Ashmead). However, it completed development only in unparasitized pupae. Mortality of the primary parasitoid due toD. himalayanuswas approximately two-thirds the mortality inflicted on the host fly.S. geminadid not discriminate between parasitized and unparasitized pupae ofA. suspensaand developed in both.C. haywardiappears to have a more restricted host range relative to chalcidoid pupal parasitoids and this may be due to its endoparasitic development.     

Egg-laying experience and acceptance of parasitized hosts by the parasitoid,Leptopilina heterotoma (Hymenoptera: Eucoilidae)

The influence of egg-laying experience on the response of females of the eucoilid parasitoid,Leptopilina heterotoma, to parasitized and unparasitizedDrosophila melanogaster host larvae was examined under more controlled conditions than those used in past studies. In laboratory assays, we precisely manipulated both the number of eggs laid by females and the kind of larvae (parasitized versus unparasitized) in which the eggs were laid. We found that the tendency to avoid laying eggs in parasitized hosts depended markedly on whether or not eggs had been laid previously, but depended little on whether those eggs had been laid in parasitized or unparasitized hosts. The observed effect of general egg-laying experience on avoidance of parasitized hosts may reflect responses to either changes in the wasp's internal state (perhaps, changes in egg load) or changes in the wasp's neural representation of the external environment (such as those presumed to occur during learning). In light of these results, we offer a tentative reinterpretation of several earlier studies.