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Information acquisition and time allocation in insect parasitoids
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Information acquisition and time allocation in insect parasitoids Jacques J.M. van Alphen1, Carlos Bernstein2 and Gerard Driessen1 1 2
Institute for Evolutionary and Ecological Sciences, P.O. Box 9516, 2300 RA Leiden, The Netherlands Biometrie et Biologie Evolutive, Universite´ Claude Bernard-Lyon 1, 43 Bld Du 11 Novembre 1918, 69622 Villeurbanne Cedex, France
All animals face the problem of finding resources for growth, maintenance and reproduction. Foraging in a heterogeneous (i.e. patchy) environment requires seemingly complex decisions, such as where to forage, and for how long. To make such decisions, animals need to acquire relevant information from their environment. Recent studies of how parasitoids acquire information and allocate their time to the exploitation of host patches use a combination of functional (evolutionary) and causal (mechanistic) approaches. They show that parasitoids can allocate foraging time to patches in an adaptive way and that members of the same species can respond differently to the same environmental cues, depending on their physiological state and previous experiences or on genetic differences. Functional models now help to explain these contrasting responses. Recent advances in the study of how animals distribute their time between the different localities (patches) where resources are available (patch-time allocation) have brought one of the classic problems of behavioural ecology into the realm of evolutionary biology and opened the field for comparative studies. We are now beginning to understand how natural selection acts on the mechanisms that control time allocation in environments that differ in structure and how information constraints determine time-allocation decisions. Understanding the behavioural mechanisms of time allocation decisions enables us to study the genetic basis of these mechanisms. We can now use a genetic approach as well as phenotypic modeling to study adaptation in foraging behaviour. Of Tinbergen’s four explanatory levels in biology [1], behavioural ecologists initially prioritized the evolutionary explanation (i.e. ultimate causes) of animal behaviour. The early models of adaptive patch exploitation considered the spatial distribution of resource availability and predicted the time allocated to different resource patches by a single individual [2] or the equilibrium distribution of a group of foragers [3]. These models were functional (i.e. predictions only considered the fitness effect for the forager) and assumed that the forager had full knowledge of resource distribution. Consequently, they did not consider the behavioural mechanisms (i.e. proximate causes) used by foragers to control the time that they spent in each patch or the mechanisms that they used to obtain information Corresponding author: Jacques J.M. van Alphen ([email protected]).
about resource distribution. Behavioural ecologists initially suggested that animals foraging in a heterogeneous environment should be able to acquire and process information, because the environment changes continuously and each individual experiences a different environment as it samples a different subset of the available patches. How they do this is a key question in the study of animal behaviour. Animals foraging in a heterogeneous environment face complex decisions. How do they decide where to forage? How do they decide if it is better to leave a patch or to continue searching it? Why do some animals respond differently to the same environmental cue? Insect parasitoids have often been used to test theory in behavioural ecology. They are important agents of natural control of herbivorous insect populations, and are often used as biological control agents in agriculture. They lay their eggs on or inside the bodies of other arthropods, mainly insects, and the larvae feed on the tissues of the host, eventually killing it to complete their development (Box 1). Female parasitoids generally start searching for hosts shortly after emergence. However, most host species are not evenly dispersed over the habitat, but tend to cluster in groups of variable size (patches) and, thus, the parasitoid female has to divide her time between different patches to maximize the number of offspring that she can produce during her short adult life. Because of the direct link between oviposition and fitness, the behavioural mechanisms that determine the time a parasitoid spends on a patch are probably subject to strong selective pressures, and parasitoid patch-time allocation has therefore received much attention from behavioural ecologists. Researchers have shown that a wide variety of environmental stimuli affect patch-time allocation in parasitoids [4], but how the foraging animal integrates this information was unknown for a long time. The information problem Animals such as mammals and birds are long lived, and can learn the geography of their home range and the profitability of different areas before beginning to reproduce. Subsequently, they must update this information either from their own experience or from observing the gains obtained by conspecifics. As newly born female parasitoids start to reproduce shortly after emergence, they lack such information and must acquire it independently whilst searching for suitable hosts. Hence, parasitoid
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Box 1. The life history of parasitoids Parasitoids are insects (usually wasps or flies) that lay eggs inside or on other insects (the hosts). Depending on the species, parasitoids attack different host stages (eggs, larvae, pupae or adults) [e.g. the wasp Venturia canescens attacks moth larvae living in flour or desiccated fruits, from the second to the fifth (and last) instar]. A larva emerges from the egg and consumes the host. Depending on the species, a single (‘solitary’ parasitoids, such as V. canescens ) or several (‘gregarious’ parasitoids, such as Tetrastichus asparagi [a]) adult parasitoids emerge. Some female parasitoids use a host for oviposition, whilst others might also use them as a food source. When males do occur (some parasitoids, such as many strains of V. canescens, are parthenogenetic), they have little interaction with the host. To parasitize a host, female parasitoids must successfully: (1) find a host patch; (2) locate the host inside the patch; and (3) identify hosts that are profitable for the development of the offspring. The different cues used by parasitoids in each of these steps are reviewed in Box 2. A specific problem for insect parasitoids, is that they leave the host in the patch after attacking it, in contrast to predators, which remove the prey after attack. This complicates the assessment of patch quality,
foraging is likely to be constrained by the information available during at least part of the adult life of the female. However, female parasitoids use a wide variety of chemical stimuli to obtain information about their environment, and this enables them to restrict their foraging behaviour to that part of the habitat in which hosts are most likely to be found. Within these suitable areas, parasitoids again use many types of cue as information for patch choice and patch-time decisions (Box 2). This enables them to forage efficiently in the absence of information about the full
given that the quality of the patch is progressively decreased but the number of hosts in the patch does not change. That attacked hosts are left in the environment makes them vulnerable to further attack by individuals of the same or other parasitoid species. Conspecific females might compete for hosts by ovipositing in an already parasitized host (superparasitism). A female can also superparasitize a host in which she herself has already oviposited (self-superparasitism). In solitary parasitoids, the parasitoid larvae in a superparasitized host will fight for the possession of the host upon emergence and only one will survive. Some parasitoids parasitize the eggs of other parasitoids (hyperparasitism).
Reference a van Alphen, J.J.M. (1980) Aspects of the foraging behaviour of Tetrastichus asparagi Crawford and Tetrastichus spec. (Eulophidae), gregarious egg parasitoids of the asparagus beetles Crioceris asparagi L. and C. duodecimpunctata L. (Chrysomelidae). I. Hostspecies selection, host-stage selection and host discrimination. Neth. J. Zool. 30, 307 – 325
distribution of hosts and host patches over the habitat. Some such cues will increase the probability that the parasitoid will stay in the patch and are called incremental, whereas others decrease this probability and are called decremental (Box 3). Mechanisms for deciding when to leave a patch Incremental effects of host encounters The key question to understanding how parasitoids allocate search time over patches in a habitat is how
Box 2. Cues that parasitoids use to obtain information Parasitoid foraging behaviour is often divided into three steps: (1) searching for and selecting habitat patches with hosts; (2) searching for hosts within the habitat; and (3) selection of profitable hosts for offspring production. Different cues are used by the parasitoid at each step.
Cues for host habitat location at a distance To find patches with hosts, parasitoids often respond to olfactory cues, which are detected by using sensillae on the antennae, and to which the parasitoids respond by flying up wind. The nature and concentration of the stimulus provide information about the identity of the host species present, and the density of hosts in the patch, or about the presence of competitors or natural enemies, such as hyperparasitoids [a,b] or predators.
Cues for patch exploitation After arrival in the patch, parasitoids often react to substances (kairomones) produced by the host, such as frass, pheromones or secretions (e.g. faeces, wax or honeydew), which can be perceived by sensillae on the antennae or on the tip of the ovipositor. The presence and concentration of kairomones can inform the parasitoid about the size of the patch and the host density [c]. In response, the movement pattern of the searching parasitoid changes, resulting in an intensive area-restricted search, because it turns inward when reaching the patch edge (recognized by an abrupt decrease in kairomone concentration) and/or because it reduces walking speed or turns more often. This response is modulated by the different experiences of the animal whilst foraging. Many parasitoids locate their hosts by drumming with their antennae on the substrate, and/or by probing the substrate with their http://tree.trends.com
ovipositor. Some parasitoids locate their hosts by reacting to vibrations produced by the host in the substrate [d], which are detected by using the legs. The use of visual cues is rare.
Cues for host selection When an individual host is encountered, it is examined either externally with the antennae, and/or internally by probing with the ovipositor. This provides the parasitoid with information about the size and quality of the host (e.g. whether it is already parasitized), which the parasitoid uses to decide whether to accept the host. If accepted, the information is also used to decide how many eggs to lay and which sex the offspring will be. If a host is accepted for oviposition, it is, in most species, marked with an external and/or internal marking substance that enables the parasitoid to recognize it as being already parasitized upon re-encounter, and to distinguish hosts parasitized by itself from hosts parasitized by competing females. Already parasitized hosts can be rejected, or parasitized for a second time (superparasitism).
References a Janssen, A. et al. (1995) Odour-mediated avoidance of competition in Drosophila parasitoids: the ghost of competition. Oikos 73, 356 – 366 b Ho¨ ller, C. et al. (1994) Enemy induced dispersal in a parasitic wasp. Experientia 50, 182 – 185 c Galis, F. and van Alphen, J.J.M. (1981) Patch time allocation and search intensity of Asobara tabida Nees (Braconidae), a larval parasitoid of Drosophila. Neth. J. Zool. 31, 596 – 611 d Djemai, I. et al. (2001) Matching host reactions to parasitoid wasp vibrations. Proc. R. Soc. Lond. Ser. B 268, 2403 – 2408
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Box 3. Incremental and decremental processes Incremental mechanism A parasitoid is said to use an incremental mechanism for decision making when each oviposition increases its probability of staying in a
(a) Responsiveness
aH2 Rich patch
aH1 Poor patch
patch. Inspired by his observations of the behaviour of the parasitoid wasp Venturia (Nemeritis ) canescens, Waage [a] suggested a mechanism for how long parasitoids decide to remain on a particular patch. Parasitoids are assumed to have a certain level of ‘responsiveness’ (tendency to stay in the patch), and the initial responsiveness is determined by the kairomone concentration, which is proportional to host number. Responsiveness decreases linearly with the time spent on the patch. As long as this responsiveness is above a given threshold, parasitoids turn inward each time they reach the edge of the patch, otherwise the patch is abandoned (Fig. Ia). An oviposition alters the waning of this response by adding an increment (I ) to the current level of responsiveness. I is assumed to be proportional to the time elapsed since the last oviposition, up to a maximum value, Imax (Fig. Ib). T, the duration of a patch visit is given by Eqn I: X aH þ li 2 r p T ¼
Time
Responsiveness
½Eqn I p
r*
(b)
i
b
aH2
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Fig. I. The Waage (1979) model [a]. (a) The initial responsiveness to the patch edge (aHi) is proportional to host density (Hi) and decreases as time in the patch proceeds. As a result of ovipositions, responsiveness increases, the increment being dependent on the time elapsed since the last oviposition. When the level of responsiveness has dropped below the critical threshold, r p, the parasitoid leaves the patch. (b) A decremental patch-leaving decision rule. The initial responsiveness to the patch edge (aHi) is proportional to host density (Hi) and decreases as time on the patch proceeds (decay is assumed linear for simplicity). In reaction to ovipositions, the responsiveness decreases. In this example decrements are taken as constant. Black arrows denote ovipositions in a relatively rich patch; red arrow denotes an oviposition in a relatively poor patch.
they integrate the different types of information available. The first mechanistic model considered the effect of several stimuli [5] and integrated the influence of kairomones (i.e. substances produced by the host) that set the initial attractiveness of the patch, the progressive habituation of the parasitoid to this stimulus, and the effect of ovipositions Box 3). Each oviposition in an unparasitized host increases the motivation of the parasitoid to stay and to continue search. (The animal is said to use an incremental mechanism.) This mechanism results in the parasite spending more time in patches with more hosts. Although this model gives a good qualitative description of patchtime allocation in many species of parasitoids, it is based on only two of the stimuli affecting patch time; that is, the kairomone and the encounters with unparasitized hosts. http://tree.trends.com
where H is the number of hosts in the patch, r is the threshold of responsiveness, a is a constant relating initial responsiveness to the number of hosts and b is the rate of responsiveness decline. Waage’s [a] model is a classic example of an incremental mechanism. Waage’s model assumes that parasitoids gain an accurate estimation of initial host availability through kairomone concentration, and improve this estimation through ovipositions (i.e. whilst the patch is getting poorer). Driessen and Bernstein [b] suggested that incremental mechanisms would be more adequate when parasitoids can detect the presence of hosts in a patch but not their number (as is the case when host numbers are high). In this case, the mechanism will lead to a longer patch residence time and to a more thorough exploitation of the richest patches.
For a decremental mechanism, responsiveness to kairomones decreases at each oviposition, which means that the parasitoid is more likely to leave a particular patch (Fig. Ib). This mechanism is adaptive only when parasitoids have a good estimation of initial host availability [b]: The estimated value of the patch declines as ovipositions render the patch poorer. This assumes that availability does not change rapidly as a consequence of conspecific foraging (T. Spataro, PhD thesis, Lyon University, 2001) or any other external causes of host mortality.
References a Waage, J.K. (1979) Foraging for patchily-distributed hosts bye the parasitoid Nemeritis canescens. J. Anim. Ecol. 48, 353– 371 b Driessen, G. and Bernstein, C. (1999) Patch departure mechanisms and optimal exploitation in an insect parasitoid. J. Anim. Ecol. 68, 445 – 459
Decremental effects of host encounters In contrast with the predictions of this model [5], ovipositions decrease patch-residence time in many parasitoids, which, therefore, are said to use a decremental mechanism. This was observed in the meal-moth larval parasitoid Venturia canescens [6,7], for which Waage [5] developed the first mechanistic model. Both incremental and decremental mechanisms are common in nature (Table 1). How could it be that in patch-leaving decisions that should be under strong selective pressure, important events such as oviposition could have an incremental effect in one species and a decremental effect in another? Which mechanism to use? Pre-dating most experimental work, Iwasa et al. [8] offered
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Table 1. Empirical evidence for species with incremental and decremental mechanisms Species with incremental mechanisms Aphidius nigriceps Ashmead Asobara tabida Nees Chrysocharis pentheus Walker Cotesia rubecula (Marshall) Dacnusa sibirica Telenga Dapsilarthra rufiventris (Nees) Encarsia formosa Gahan Leptopilina heterotoma (Thompson) Leptopilina clavipes (Hartig) Opidius dimidiatus (Ashmead) Trichogramma brassicae Venturia canescens (Gravenhorst) a
Species with decremental mechanisms [40] [41] [42] [26] [43] [20] [44] [15,45] [14] [46] [13] [5]
Aphidius colemani Viereck Aphidius rhopalosiphi (De Stefani-Peres) Cardiochiles nigripes Viereck Cotesia rubecula (Marshall) Diadegma semiclausum (Helle´ n) Diaeretiella rapae MacIntosh Sympiesis seriseicornis Nees Telenomus busseolae (Gahan) Venturia canescens (Gravenhorst)
[47] a
[48] [25] [49] [50] [51] [16] [7]
The mechanism used depends on the number of eggs previously laid.
the first explanation. Their model suggests that the kind of mechanism that parasitoids use depends on the distribution of the hosts. Parasitoids foraging for hosts with an aggregated distribution (high variability in the number of host per patch) should use incremental mechanisms, whereas those foraging for uniformly distributed hosts (low variability in the number of hosts per patch) should use decremental mechanisms. Parasitoids foraging for Poisson-distributed hosts (a mathematical assumption rather than a natural observation) should be indifferent to the number of eggs that they have laid. This model is based on the assumption that the type of host distribution is constant over generations and that there is selection for the appropriate mechanism. Nevertheless, short-term changes in the environment occur during the lifetime of individuals and they have evolved mechanisms to gather information to update their knowledge. When the number of hosts in a patch is known (e.g. when the kairomone concentration is a reliable indicator of the number of hosts in the patch), each oviposition implies a subsequent decrease in host availability. The patch becomes progressively less valuable compared with the rest of the environment and animals should use a decremental mechanism. Such a mechanism is also superior to a ‘fixed number rule’ (i.e. leave patch after x hosts have been found), because it enables a parasitoid to deal with the variation in host numbers which, although small, is always present. However, when information about host availability is unreliable (e.g. some patches are very rich, other extremely poor, but no specific cue is available), the timing of each additional oviposition reveals the quality of the patch and determines whether a parasitoid should continue to search it. In this case, an incremental mechanism would be expected. This idea was pursued both theoretically and experimentally by Driessen and Bernstein [6], who first showed that the hosts of V. canescens tend to have a uniform distribution in the field (e.g. carob fruits attacked by the moth Ectomyelois ceratoniae, a host of V. canescens, almost always contain a single host). They then showed that V. canescens obtains, at arrival in a patch, a reliable estimation of the host density by detecting the kairomone concentration. Moreover, they showed in an optimization model that for V. canescens searching individually, a http://tree.trends.com
decremental mechanism will be out-competed by an incremental one only when travel times between patches are much larger than those that are likely to occur in the field [6]. However, elaborating on this work, and using a modeling approach, Spataro (T. Spataro, PhD thesis, Lyon University, 2001) showed that when parasitoid density is high, kairomone concentration and host distribution no longer provide reliable information: host patches might have already been exploited by others and the hosts might already be parasitized. In this case, parasitoids should use an incremental mechanism. In the field, parasitoids might use cues other than kairomones to assess patch quality when the presence of competitors makes the kairomone concentration an unreliable predictor of patch quality. Marking pheromones deposited by conspecifics, contacts with parasitized hosts, or odours produced by the competitors might provide such cues. A switch from an incremental to a decremental rule occurs in the parasitoid Aphidius rhopalosiphi (Y. Outreman, PhD thesis, Rennes University, 2000). The parasitoid begins by using an incremental rule when exploiting an aggregation of wheat aphids Sitobion avenae, but switches to a decremental rule when the patch has been partly exploited. This results in the parasitoid leaving the patch long before all the hosts have been parasitized. As aphids become more and more defensive during the visit of the parasitoid, the probability that the latter becomes immobilized by a sticky substance ejected by the aphids increases. Hence, the accelerated departure decreases the mortality risk of the parasitoid [9]. Most of our knowledge about the responses of parasitoids to host encounters stems from using statistical methods that enable us to determine quantitatively the contribution of the different types of information to the instantaneous probability of leaving the patch. This became possible by the introduction [10] of the use of Cox’s proportional hazard model [11,12] into behavioural ecology, which quantifies and integrates different processes and measures how each of them contributes to the determination of patch time (Box 4). We have therefore progressed from the qualitative assessment of the influence of isolated stimuli to a more quantitative analysis, the results of which can be integrated into mechanistic or adaptive patch models [7,13]. For example, one could ask what are the optimal values of the parameters
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Box 4. Cox’s Proportional Hazards model People die, laboratory glassware breaks, parasitoids leave patches. In all these cases, something (someone) disappears. If this process happens at a constant rate, l, in deterministic terms, we would observe that the change in number over time (dN/dt ), ¼ lN, where N refers to the number (e.g. Asobara tabida females in a patch of Drosophila larvae). In probabilistic terms, mean time of disappearance is 1/l. When l is not constant but a function of time and the outcome of other intervening processes, the maths become more complicated. The proportional hazards model (and other related techniques) enables us to estimate how l is affected by different events (or covariates) and their precise timing, being for instance encounters with hosts or conspecifics. l is given as l(t,z), where z is a vector, t is the time (since the observations began, for instance). Individual zi, the covariates, might be continuous or discrete variables and might depend on time [in this case we will write zi(t )]. In 1985, Haccou and Hemerik [a] introduced into behavioural research, a statistical technique known as Proportional Hazards Analysis or Cox model, which had been used successfully in medical research to study mortality rates and to assess the effect on survival of different treatments. This technique estimates l(t,z) as (Eqn I) ! X lðt; zÞ ¼ l0 ðtÞexp bi z i ðtÞ ½Eqn I i
representing the influence of different stimuli, thus linking the causal questions to functional, evolutionary ones. The proportional hazards model has now been applied to several data sets representing a variety of parasitoid species. They include the Drosophila parasitoids Leptopilina clavipes [14] and Leptopilina heterotoma [15], V. canescens [6,7], the egg parasitoids Trichogramma brassicae and Telenomus busseolus [13,16] and the aphid parasitoid Aphidius rhopalosiphi (Y. Outreman, PhD thesis, Rennes University, 2000). Other cues affecting patch time In addition to contact kairomones and encounters with hosts, several other cues have been shown to affect patch time in parasitoids, demonstrating that foraging decisions in parasitoids are based on the assimilation of many different sorts of information. For example, the females of several parasitoid species leave a marking substance on the substrate whilst searching, and, when a female visits a patch already searched, either by herself or by a different female, she responds to the marking substance by leaving sooner in comparison with unmarked patches (i.e. encounters with the marking substance have a decremental effect) [17 – 19]. Sugimoto [20] proposed a mechanism for time allocation based on the assumption that marking pheromone concentration will increase with time in a patch. When the concentration increases above a certain threshold, the female abandons the patch. However, ovipositions would increase this leaving threshold. Decremental effects of encounters with already parasitized hosts have also been documented [13,14,16] (Y. Outreman, PhD thesis, Rennes University, 2000). This might be especially important for parasitoids searching on patches simultaneously with competitors, or on patches that have been previously visited by one or more competitors. Encounters with parasitized hosts can also http://tree.trends.com
where l0(t ) is an (unspecified) base-line rate assumed to depend only on time and is common to all possible outcomes [l0(t ) corresponds to the situation in which all covariates are set to zero] and bi are parameters. The exponential is used to assure that l(t,z) will always take positive values. For a parasitoid, t could be the time since arrival to the patch or since the last egg was laid, zi(t ) could be the number of eggs already laid, the number of conspecifics in the patch, and so on. Nonsignificant bi values correspond to processes that do not influence the outcome (e.g. patch leaving). Positive (negative) bi values will reveal processes (number of encounters with parasitized hosts, for instance) that increase (decrease) the leaving rate, so animals stay shorter (longer) times. This technique enables us to partition the influence of different processes with a minimum of a priori decisions.
Reference a Haccou, P. and Hemerik, L. (1985) The influence of larval dispersal in the cinnabar moth (Tyria jacobaea ) on predation by the red wood ant (Formica polyctena ). An analysis based on the proportional hazards model. J. Anim. Ecol. 54, 755 – 769
provide information about the current level of patch exploitation and hence about when to leave a patch. Different responses to parasitized and healthy hosts are possible only if a parasitoid can discriminate between the two. Most parasitoids have this ability, but others oviposit in each host encountered. Hosts can therefore become parasitized several times (superparasitism). The lack of host discrimination in a parasitoid can be considered as an information constraint [21]. Optimal patch time under this constraint is predicted to be shorter than without the constraint, because patches become unprofitable sooner when self-superparasitism cannot be detected and avoided. Other events, such as encounters with other parasitoids, could also result in either incremental or decremental effects on patch time, as shown for L. heterotoma [22]. Compared with females that spent the previous day alone, females that had spent the previous day with competitors stayed longer on patches and superparasitized several hosts when foraging alone the following day. This occurred because the probability of gaining offspring from a given host is proportional to the number of eggs laid on it. Thus by self-superparasitizing several hosts, the female makes the patch less attractive for competitors that find the patch after she has left and increases the probability of her producing offspring from the superparasitized hosts. In Asobara tabida, also a parasitoid of Drosophila larvae, both the quality of the previous patch and the time elapsed since the previous patch visit affects the time spent on a patch [23] in accordance with the predictions of classic optimal foraging theory [2]. The females stayed longer on the next patch after a visit to a low-quality patch and after more time had elapsed since the previous patch visit [23]. The probability of leaving a patch also increases as the number of successive patches already visited increases [16,24 – 26]. By contrast, female A. rhopalosiphi that have
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already visited a high-quality patch spend more time in the next patch (Y. Outreman, PhD thesis, Rennes University, 2000). The function of this change in behaviour remains unclear. Exposure to circumstances that indicate unfavourable environmental conditions in near future (e.g. dropping air pressure heralding a thunderstorm and low temperatures and short day length heralding the onset of winter) result in longer patch times [27,28].
Individual variation in patch leaving Internal state The internal state of a parasitoid (e.g. egg load, and lipid and carbohydrate reserves) might also provide information about future life span and affect patch time. However, few studies of parasitoid patch-leaving decisions have used a state-dependent approach [27–29] (i.e. assuming that optimal decisions will depend on the state of the animal). This approach was also used in a theoretical study of how a parasitoid should allocate its foraging time between host patches and the search of metabolic resources [30], but there are no experimental tests. The little evidence available suggests that at least in some parasitoid species, no lipogenesis occurs in the adults and that energy reserves during adult life can only be supplemented in the form of carbohydrates [31–33]. This adds a new twist to the problem by suggesting that in state-dependent models, metabolic reserves should not be represented as a single variable.
Genetic variation in patch-time allocation That patch-leaving decision rules are subject to natural selection assumes that the mechanisms are under genetic control and that there is or has been genetic variability. Indeed, genetic variation has been demonstrated in the responses of T. busseolae (a parasitoid that uses a decremental rule) to ovipositions and encounters with parasitized hosts [16]. However, this raises the question of how genetic variation is maintained in nature. The answer could be that intra- and inter-generation stochastic processes ensure that individuals experience a different environment as they sample a different subset of available patches, hence, selection within a generation would be weak and the direction of selection would fluctuate between generations.
Foraging in groups: superparasitism and time allocation Competition between adult females on a patch is usually by superparasitism, as we describe above. In a superparasitized host, the larvae of solitary parasitoids will also compete for the possession of the host. The winning larva kills the other(s). In gregarious parasitoids (i.e. competing larvae do not kill each other), superparasitism results in smaller, less-fit parasitoids emerging from that host. In spite of this, in both types of parasitoid, a female ovipositing in a host already parasitized by a competing female might still obtain offspring. Hence, superparasitism can be advantageous in circumstances where better alternatives (i.e. unparasitized hosts), are scarce. A special http://tree.trends.com
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situation occurs when competing parasitoids exploit a patch simultaneously. A female leaving before the others would leave the hosts that she has parasitized available for superparasitism. This would result in a loss of offspring unless she also stayed longer and compensated for the loss of offspring by superparasitizing herself. This results in all the females staying longer. Experimental evidence for this comes from studies of L. heterotoma [34] and A. tabida [35]. It is unknown which mechanism leads the females to stay longer. There are clear indications that odours or physical contacts could play a role [34]. Alternatively, the information about the presence of conspecific parasitoids could come from the hosts themselves. The ability to recognize hosts that are parasitized by conspecifics from hosts parasitized by the parasitoid itself has been reported in several species e.g. V. canescens [36] and Epidinocarsis lopezi [17]. Parasitoids could respond to these types of cue by changing the strength or direction of their response to host encounters. Theory about group foraging by parasitoids in depletable patches has not progressed since the early 1990s [37,38] and is one topic for which there are neither theoretical developments nor experimental tests [39]. However, it is one of the most promising avenues for future research.
Conclusion In a heterogeneous environment, animals must acquire and process information to forage efficiently because the environment changes continuously. To make adaptive decisions, animals have to compare alternatives that present themselves in a sequential manner or actual values with what they have experienced as being the mean values for the environment as a whole. We now know that parasitoids acquire and integrate information from a large variety of sources. Thus, the mechanisms involved in information acquisition and processing can be included in functional models, enabling us to predict the evolutionary consequence of the use of different mechanisms. Some of the most promising subjects for future research are the studies of state-dependent patch-leaving decisions, group foraging and the influence of experiences during previous patch visit(s). New emerging fields of research include the behavioural genetics of foraging behaviour, the optimal values of incremental and decremental responses to different stimuli and the question of to what extent parasitoids in nature are constrained by their lack of information about the spatial distribution of hosts and competitors. Current knowledge already shows that insect parasitoids are an ideal model with which to study how natural selection shapes foraging behaviour under the constraint of limited information about the environment.
Acknowledgements We thank Eric Wajnberg for stimulating discussion and Emmanuel Desouhant, Imen Djemai, Alex Kacelnik, Bart Pannebakker and two anonymous referees for suggesting improvements.
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References 1 Tinbergen, N. (1963) On aims and methods of ethology. Z. Tierpsychol. 20, 410 – 433 2 Charnov, E.L. (1976) Optimal foraging: the marginal value theorem. Theor. Popul. Biol. 9, 129 – 136 3 Fretwell, S.D. and Lucas, H.L. (1970) On territorial behaviour and other factors in habitat distribution in birds. Acta Biotheor. 19, 16 – 36 4 Godfray, H.C.J. (1994) Parasitoids, Behavioral and Evolutionary Ecology, Princeton University Press 5 Waage, J.K. (1979) Foraging for patchily-distributed hosts bye the parasitoid Nemeritis canescens. J. Anim. Ecol. 48, 353 – 371 6 Driessen, G. and Bernstein, C. (1999) Patch departure mechanisms and optimal exploitation in an insect parasitoid. J. Anim. Ecol. 68, 445 – 459 7 Driessen, G. et al. (1995) A count-down mechanism for host search in the parasitoid Venturia canescens. J. Anim. Ecol. 64, 117 – 125 8 Iwasa, Y. et al. (1981) Prey distribution as a factor determining the choice of optimal foraging strategy. Am. Nat. 117, 710 – 723 9 Outreman, Y. et al. (2001) Can imperfect host discrimination explain partial patch exploitation in parasitoids? Ecol. Entomol. 26, 277– 280 10 Haccou, P. and Hemerik, L. (1985) The influence of larval dispersal in the cinnabar moth (Tyria jacobaea ) on predation by the red wood ant (Formica polyctena ). An analysis based on the proportional hazards model. J. Anim. Ecol. 54, 755– 769 11 Cox, D.R. (1972) Regression models and life tables. Biometrics 38, 67 – 77 12 Cox, D.R. and Oakes, D. (1984) Analysis of Survival Data, Chapman & Hall 13 Wajnberg, E. et al. (2000) Patch leaving decision rules and the Marginal Value Theorem: an experimental analysis and a simulation model. Behav. Ecol. 11, 577 – 586 14 Hemerik, L. et al. (1993) Effects of intra-patch experiences on patch time, search time and searching efficiency of the parasitoid Leptopilina clavipes. J. Anim. Ecol. 62, 33 – 44 15 Haccou, P. et al. (1991) Information processing by foragers: effects of intra-patch experiences on the leaving tendency of Leptopilina heterotoma. J. Anim. Ecol. 60, 93 – 106 16 Wajnberg, E. et al. (1999) Genetic variation in patch time allocation in a parasitic wasp. J. Anim. Ecol. 68, 121 – 133 17 van Dijken, M.J. et al. (1992) Recognition of individual-specific marked hosts by the solitary parasitoid Epidinocarsis lopezi. Behav. Ecol. Sociobiol. 30, 77– 82 18 Ho¨ ller, C. and Hormann, R. (1993) Patch marking in the aphid hyperparasitoid, Dendrocerus carpenteri: the information contained in patch marks. Oecologia 94, 128 19 Bernstein, C. and Driessen, G. (1996) Patch marking and optimal search patterns in the parasitoid Venturia canescens. J. Anim. Ecol. 65, 211 – 219 20 Sugimoto, T. et al. (1987) Foraging for patchily-distributed leaf-miners by the parasitoid Dapsilartha rufiventris (Hymenoptera: Braconidae). II Stopping rule for host search. J. Ethol. 5, 95 – 103 21 Rosenheim, J.A. and Mangel, M. (1994) Patch leaving rules for parasitoids with imperfect hot discrimination. Ecol. Entomol. 19, 374– 380 22 Visser, M.E. et al. (1992) Adaptive superparasitism and patch time allocation in solitary parasitoids: an ESS model. J. Anim. Ecol. 61, 93 – 101 23 Thiel, A. and Hoffmeister, T.S. (2001) Wirtssuchverhalten der Brackwespe Asobara tabida in einem komplexen Habitat. Mitt. Dtsch. Ges. allg. angew. Ent. 13, 73– 76 24 Tenhumberg, B. et al. (2001) Using Cox’s proportional hazard models to implement optimal strategies: en example from behavioural ecology. Math. Comput. Model 33, 597– 607 25 Tenhumberg, B. et al. (2001) Optimal patch leaving behaviour: a case study using the parasitoid Cotesia rubecula. J. Anim. Ecol. 70, 683 – 691 26 Vos, M. et al. (1998) Patch exploitation by the parasitoids Cotesia rubecula and Cotesia glomerata in multi-patch environments with different hosts distributions. J. Anim. Ecol. 67, 774 – 783
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27 Roitberg, B.D. et al. (1992) Seasonal dynamic shifts in patch exploitation by parasitic wasps. Behav. Ecol. 3, 156 – 165 28 Roitberg, B.D. et al. (1993) Life expectancy and reproduction. Nature 36, 108 29 Keasar, T. et al. (2001) Early oviposition experience affects patch residence time in a foraging parasitoid. Entomol. Exp. Appl. 98, 123– 132 30 Sirot, E. and Bernstein, C. (1996) Time sharing between host searching and food searching in solitary parasitoids: state dependent optimal strategies. Behav. Ecol. 7, 189 – 194 31 Olson, D.M. et al. (2000) Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. Physiol. Entomol. 25, 17– 26 32 Ellers, J. (1996) Fat and eggs: an alternative method to measure the trade-off between survival and reproduction in insect parasitoids. Neth. J. Zool. 46, 227 – 235 33 Rivero, A. and West, S.A. (2002) The physiological costs of being small in a parasitic wasp. Evol. Ecol. Res. 4, 407– 420 34 Visser, M.E. et al. (1990) Adaptive superparasitism and patch time allocation in solitary parasitoid: the influence of the number of parasitoids depleting the patch. Behaviour 114, 21– 36 35 van Alphen, J.J.M. et al. (1992) Adaptive superparasitism and patch time allocation in solitary parasitoids: searching in groups versus sequential patch visits. Funct. Ecol. 6, 528– 535 36 Marris, G.C. et al. (1996) The perception of genetic similarity by the solitary parthenogenic parasitoid Venturia canescens, and its effects on the occurrence of superparasitism. Entomol. Exp. Appl. 78, 167 – 174 37 Alphen Van, J.J.M. and Visser, M.E. (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annu. Rev. Entomol. 35, 59 – 79 38 Sjerps, M. and Haccou, P. (1994) Effects of competition on optimal patch leaving: a war of attrition. Theor. Popul. Biol. 46, 300– 318 39 Giraldeau, L.A. and Caraco, T. (2000) Social Foraging Theory, Princeton University Press 40 Cloutier, C. and Bauduin, F. (1990) Searching behavior of the aphid parasitoid Aphidius nigripes (Hymenoptera: Aphidiidae) foraging on potato plants. Environ. Entomol. 19, 222– 228 41 van Alphen, J.J.M. and Galis, F. (1983) Patch time allocation and parasitization efficiency of Asobara tabida, a larval parasitoid of Drosophila. J. Anim. Ecol. 52, 937 – 952 42 Sugimoto, T. and Tsujimoto, S. (1988) Stopping rule for host search by the parasitoid, Chrysocharis pentheus (Hymenoptera: Eulophidae), in host patches. Res. Popul. Ecol. 30, 123– 133 43 Sugimoto, T. et al. (1990) Foraging for patchily-distributed leaf-miners by the parasitic wasp, Dacnusa sibirica. Res. Popul. Ecol. 32, 387 – 389 44 van Roermund, H.J.W. et al. (1994) Influence of intra-patch experiences and temperature on the time allocation of the whitefly parasitoid Encarsi formosa (Hymenoptera: Aphelinidae). J. Insect Behav. 7, 483– 501 45 Lenteren, J.C. and Bakker, K. (1978) Behavioural aspects of the functional response of a parasite (Pseudeudeucoila bocheri Weld) to its host (Drosophila melanogaster ). Neth. J. Zool. 28, 213– 233 46 Nelson, J.M. and Roitberg, B.D. (1995) Flexible patch time allocation by the leafminer parasitoid, Opius dimidiatus. Ecol. Entomol. 20, 245– 252 47 van Steenis, M.J. et al. (1996) Time allocation of the parasitoid Aphidius colemani foraging for Aphis gossypii on cucumber leaves. J. Insect Behav. 9, 283 – 295 48 Strand, M.R. and Vinson, B. (1982) Behavioural response of the parasitoid Cardiochiles nigriticeps to a kairomone. Entomol. Exp. Appl. 31, 308 – 315 49 Wang, X. (2002) Patch exploitation by the parasitoids of Plutella xylostella (L.): from individual behaviour to population dynamics. Aust. J. Entomol. 41, 281– 282 50 Shaltiel, L. and Ayal, Y. (1998) The use of kairomones for foraging decisions by an aphid parasitoid in small host aggregations. Ecol. Entomol. 23, 319 – 329 51 Casas, J. et al. (1993) A probabilistic model for the functional response of a parasitoid at the behavioural time-scale. J. Anim. Ecol. 62, 194– 204
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Information acquisition and time allocation in insect parasitoids Jacques J.M. van Alphen1, Carlos Bernstein2 and Gerard Driessen1 1 2
Institute for Evolutionary and Ecological Sciences, P.O. Box 9516, 2300 RA Leiden, The Netherlands Biometrie et Biologie Evolutive, Universite´ Claude Bernard-Lyon 1, 43 Bld Du 11 Novembre 1918, 69622 Villeurbanne Cedex, France
All animals face the problem of finding resources for growth, maintenance and reproduction. Foraging in a heterogeneous (i.e. patchy) environment requires seemingly complex decisions, such as where to forage, and for how long. To make such decisions, animals need to acquire relevant information from their environment. Recent studies of how parasitoids acquire information and allocate their time to the exploitation of host patches use a combination of functional (evolutionary) and causal (mechanistic) approaches. They show that parasitoids can allocate foraging time to patches in an adaptive way and that members of the same species can respond differently to the same environmental cues, depending on their physiological state and previous experiences or on genetic differences. Functional models now help to explain these contrasting responses. Recent advances in the study of how animals distribute their time between the different localities (patches) where resources are available (patch-time allocation) have brought one of the classic problems of behavioural ecology into the realm of evolutionary biology and opened the field for comparative studies. We are now beginning to understand how natural selection acts on the mechanisms that control time allocation in environments that differ in structure and how information constraints determine time-allocation decisions. Understanding the behavioural mechanisms of time allocation decisions enables us to study the genetic basis of these mechanisms. We can now use a genetic approach as well as phenotypic modeling to study adaptation in foraging behaviour. Of Tinbergen’s four explanatory levels in biology [1], behavioural ecologists initially prioritized the evolutionary explanation (i.e. ultimate causes) of animal behaviour. The early models of adaptive patch exploitation considered the spatial distribution of resource availability and predicted the time allocated to different resource patches by a single individual [2] or the equilibrium distribution of a group of foragers [3]. These models were functional (i.e. predictions only considered the fitness effect for the forager) and assumed that the forager had full knowledge of resource distribution. Consequently, they did not consider the behavioural mechanisms (i.e. proximate causes) used by foragers to control the time that they spent in each patch or the mechanisms that they used to obtain information Corresponding author: Jacques J.M. van Alphen ([email protected]).
about resource distribution. Behavioural ecologists initially suggested that animals foraging in a heterogeneous environment should be able to acquire and process information, because the environment changes continuously and each individual experiences a different environment as it samples a different subset of the available patches. How they do this is a key question in the study of animal behaviour. Animals foraging in a heterogeneous environment face complex decisions. How do they decide where to forage? How do they decide if it is better to leave a patch or to continue searching it? Why do some animals respond differently to the same environmental cue? Insect parasitoids have often been used to test theory in behavioural ecology. They are important agents of natural control of herbivorous insect populations, and are often used as biological control agents in agriculture. They lay their eggs on or inside the bodies of other arthropods, mainly insects, and the larvae feed on the tissues of the host, eventually killing it to complete their development (Box 1). Female parasitoids generally start searching for hosts shortly after emergence. However, most host species are not evenly dispersed over the habitat, but tend to cluster in groups of variable size (patches) and, thus, the parasitoid female has to divide her time between different patches to maximize the number of offspring that she can produce during her short adult life. Because of the direct link between oviposition and fitness, the behavioural mechanisms that determine the time a parasitoid spends on a patch are probably subject to strong selective pressures, and parasitoid patch-time allocation has therefore received much attention from behavioural ecologists. Researchers have shown that a wide variety of environmental stimuli affect patch-time allocation in parasitoids [4], but how the foraging animal integrates this information was unknown for a long time. The information problem Animals such as mammals and birds are long lived, and can learn the geography of their home range and the profitability of different areas before beginning to reproduce. Subsequently, they must update this information either from their own experience or from observing the gains obtained by conspecifics. As newly born female parasitoids start to reproduce shortly after emergence, they lack such information and must acquire it independently whilst searching for suitable hosts. Hence, parasitoid
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Box 1. The life history of parasitoids Parasitoids are insects (usually wasps or flies) that lay eggs inside or on other insects (the hosts). Depending on the species, parasitoids attack different host stages (eggs, larvae, pupae or adults) [e.g. the wasp Venturia canescens attacks moth larvae living in flour or desiccated fruits, from the second to the fifth (and last) instar]. A larva emerges from the egg and consumes the host. Depending on the species, a single (‘solitary’ parasitoids, such as V. canescens ) or several (‘gregarious’ parasitoids, such as Tetrastichus asparagi [a]) adult parasitoids emerge. Some female parasitoids use a host for oviposition, whilst others might also use them as a food source. When males do occur (some parasitoids, such as many strains of V. canescens, are parthenogenetic), they have little interaction with the host. To parasitize a host, female parasitoids must successfully: (1) find a host patch; (2) locate the host inside the patch; and (3) identify hosts that are profitable for the development of the offspring. The different cues used by parasitoids in each of these steps are reviewed in Box 2. A specific problem for insect parasitoids, is that they leave the host in the patch after attacking it, in contrast to predators, which remove the prey after attack. This complicates the assessment of patch quality,
foraging is likely to be constrained by the information available during at least part of the adult life of the female. However, female parasitoids use a wide variety of chemical stimuli to obtain information about their environment, and this enables them to restrict their foraging behaviour to that part of the habitat in which hosts are most likely to be found. Within these suitable areas, parasitoids again use many types of cue as information for patch choice and patch-time decisions (Box 2). This enables them to forage efficiently in the absence of information about the full
given that the quality of the patch is progressively decreased but the number of hosts in the patch does not change. That attacked hosts are left in the environment makes them vulnerable to further attack by individuals of the same or other parasitoid species. Conspecific females might compete for hosts by ovipositing in an already parasitized host (superparasitism). A female can also superparasitize a host in which she herself has already oviposited (self-superparasitism). In solitary parasitoids, the parasitoid larvae in a superparasitized host will fight for the possession of the host upon emergence and only one will survive. Some parasitoids parasitize the eggs of other parasitoids (hyperparasitism).
Reference a van Alphen, J.J.M. (1980) Aspects of the foraging behaviour of Tetrastichus asparagi Crawford and Tetrastichus spec. (Eulophidae), gregarious egg parasitoids of the asparagus beetles Crioceris asparagi L. and C. duodecimpunctata L. (Chrysomelidae). I. Hostspecies selection, host-stage selection and host discrimination. Neth. J. Zool. 30, 307 – 325
distribution of hosts and host patches over the habitat. Some such cues will increase the probability that the parasitoid will stay in the patch and are called incremental, whereas others decrease this probability and are called decremental (Box 3). Mechanisms for deciding when to leave a patch Incremental effects of host encounters The key question to understanding how parasitoids allocate search time over patches in a habitat is how
Box 2. Cues that parasitoids use to obtain information Parasitoid foraging behaviour is often divided into three steps: (1) searching for and selecting habitat patches with hosts; (2) searching for hosts within the habitat; and (3) selection of profitable hosts for offspring production. Different cues are used by the parasitoid at each step.
Cues for host habitat location at a distance To find patches with hosts, parasitoids often respond to olfactory cues, which are detected by using sensillae on the antennae, and to which the parasitoids respond by flying up wind. The nature and concentration of the stimulus provide information about the identity of the host species present, and the density of hosts in the patch, or about the presence of competitors or natural enemies, such as hyperparasitoids [a,b] or predators.
Cues for patch exploitation After arrival in the patch, parasitoids often react to substances (kairomones) produced by the host, such as frass, pheromones or secretions (e.g. faeces, wax or honeydew), which can be perceived by sensillae on the antennae or on the tip of the ovipositor. The presence and concentration of kairomones can inform the parasitoid about the size of the patch and the host density [c]. In response, the movement pattern of the searching parasitoid changes, resulting in an intensive area-restricted search, because it turns inward when reaching the patch edge (recognized by an abrupt decrease in kairomone concentration) and/or because it reduces walking speed or turns more often. This response is modulated by the different experiences of the animal whilst foraging. Many parasitoids locate their hosts by drumming with their antennae on the substrate, and/or by probing the substrate with their http://tree.trends.com
ovipositor. Some parasitoids locate their hosts by reacting to vibrations produced by the host in the substrate [d], which are detected by using the legs. The use of visual cues is rare.
Cues for host selection When an individual host is encountered, it is examined either externally with the antennae, and/or internally by probing with the ovipositor. This provides the parasitoid with information about the size and quality of the host (e.g. whether it is already parasitized), which the parasitoid uses to decide whether to accept the host. If accepted, the information is also used to decide how many eggs to lay and which sex the offspring will be. If a host is accepted for oviposition, it is, in most species, marked with an external and/or internal marking substance that enables the parasitoid to recognize it as being already parasitized upon re-encounter, and to distinguish hosts parasitized by itself from hosts parasitized by competing females. Already parasitized hosts can be rejected, or parasitized for a second time (superparasitism).
References a Janssen, A. et al. (1995) Odour-mediated avoidance of competition in Drosophila parasitoids: the ghost of competition. Oikos 73, 356 – 366 b Ho¨ ller, C. et al. (1994) Enemy induced dispersal in a parasitic wasp. Experientia 50, 182 – 185 c Galis, F. and van Alphen, J.J.M. (1981) Patch time allocation and search intensity of Asobara tabida Nees (Braconidae), a larval parasitoid of Drosophila. Neth. J. Zool. 31, 596 – 611 d Djemai, I. et al. (2001) Matching host reactions to parasitoid wasp vibrations. Proc. R. Soc. Lond. Ser. B 268, 2403 – 2408
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Box 3. Incremental and decremental processes Incremental mechanism A parasitoid is said to use an incremental mechanism for decision making when each oviposition increases its probability of staying in a
(a) Responsiveness
aH2 Rich patch
aH1 Poor patch
patch. Inspired by his observations of the behaviour of the parasitoid wasp Venturia (Nemeritis ) canescens, Waage [a] suggested a mechanism for how long parasitoids decide to remain on a particular patch. Parasitoids are assumed to have a certain level of ‘responsiveness’ (tendency to stay in the patch), and the initial responsiveness is determined by the kairomone concentration, which is proportional to host number. Responsiveness decreases linearly with the time spent on the patch. As long as this responsiveness is above a given threshold, parasitoids turn inward each time they reach the edge of the patch, otherwise the patch is abandoned (Fig. Ia). An oviposition alters the waning of this response by adding an increment (I ) to the current level of responsiveness. I is assumed to be proportional to the time elapsed since the last oviposition, up to a maximum value, Imax (Fig. Ib). T, the duration of a patch visit is given by Eqn I: X aH þ li 2 r p T ¼
Time
Responsiveness
½Eqn I p
r*
(b)
i
b
aH2
Rich patch
aH1
Poor patch
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Fig. I. The Waage (1979) model [a]. (a) The initial responsiveness to the patch edge (aHi) is proportional to host density (Hi) and decreases as time in the patch proceeds. As a result of ovipositions, responsiveness increases, the increment being dependent on the time elapsed since the last oviposition. When the level of responsiveness has dropped below the critical threshold, r p, the parasitoid leaves the patch. (b) A decremental patch-leaving decision rule. The initial responsiveness to the patch edge (aHi) is proportional to host density (Hi) and decreases as time on the patch proceeds (decay is assumed linear for simplicity). In reaction to ovipositions, the responsiveness decreases. In this example decrements are taken as constant. Black arrows denote ovipositions in a relatively rich patch; red arrow denotes an oviposition in a relatively poor patch.
they integrate the different types of information available. The first mechanistic model considered the effect of several stimuli [5] and integrated the influence of kairomones (i.e. substances produced by the host) that set the initial attractiveness of the patch, the progressive habituation of the parasitoid to this stimulus, and the effect of ovipositions Box 3). Each oviposition in an unparasitized host increases the motivation of the parasitoid to stay and to continue search. (The animal is said to use an incremental mechanism.) This mechanism results in the parasite spending more time in patches with more hosts. Although this model gives a good qualitative description of patchtime allocation in many species of parasitoids, it is based on only two of the stimuli affecting patch time; that is, the kairomone and the encounters with unparasitized hosts. http://tree.trends.com
where H is the number of hosts in the patch, r is the threshold of responsiveness, a is a constant relating initial responsiveness to the number of hosts and b is the rate of responsiveness decline. Waage’s [a] model is a classic example of an incremental mechanism. Waage’s model assumes that parasitoids gain an accurate estimation of initial host availability through kairomone concentration, and improve this estimation through ovipositions (i.e. whilst the patch is getting poorer). Driessen and Bernstein [b] suggested that incremental mechanisms would be more adequate when parasitoids can detect the presence of hosts in a patch but not their number (as is the case when host numbers are high). In this case, the mechanism will lead to a longer patch residence time and to a more thorough exploitation of the richest patches.
For a decremental mechanism, responsiveness to kairomones decreases at each oviposition, which means that the parasitoid is more likely to leave a particular patch (Fig. Ib). This mechanism is adaptive only when parasitoids have a good estimation of initial host availability [b]: The estimated value of the patch declines as ovipositions render the patch poorer. This assumes that availability does not change rapidly as a consequence of conspecific foraging (T. Spataro, PhD thesis, Lyon University, 2001) or any other external causes of host mortality.
References a Waage, J.K. (1979) Foraging for patchily-distributed hosts bye the parasitoid Nemeritis canescens. J. Anim. Ecol. 48, 353– 371 b Driessen, G. and Bernstein, C. (1999) Patch departure mechanisms and optimal exploitation in an insect parasitoid. J. Anim. Ecol. 68, 445 – 459
Decremental effects of host encounters In contrast with the predictions of this model [5], ovipositions decrease patch-residence time in many parasitoids, which, therefore, are said to use a decremental mechanism. This was observed in the meal-moth larval parasitoid Venturia canescens [6,7], for which Waage [5] developed the first mechanistic model. Both incremental and decremental mechanisms are common in nature (Table 1). How could it be that in patch-leaving decisions that should be under strong selective pressure, important events such as oviposition could have an incremental effect in one species and a decremental effect in another? Which mechanism to use? Pre-dating most experimental work, Iwasa et al. [8] offered
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Table 1. Empirical evidence for species with incremental and decremental mechanisms Species with incremental mechanisms Aphidius nigriceps Ashmead Asobara tabida Nees Chrysocharis pentheus Walker Cotesia rubecula (Marshall) Dacnusa sibirica Telenga Dapsilarthra rufiventris (Nees) Encarsia formosa Gahan Leptopilina heterotoma (Thompson) Leptopilina clavipes (Hartig) Opidius dimidiatus (Ashmead) Trichogramma brassicae Venturia canescens (Gravenhorst) a
Species with decremental mechanisms [40] [41] [42] [26] [43] [20] [44] [15,45] [14] [46] [13] [5]
Aphidius colemani Viereck Aphidius rhopalosiphi (De Stefani-Peres) Cardiochiles nigripes Viereck Cotesia rubecula (Marshall) Diadegma semiclausum (Helle´ n) Diaeretiella rapae MacIntosh Sympiesis seriseicornis Nees Telenomus busseolae (Gahan) Venturia canescens (Gravenhorst)
[47] a
[48] [25] [49] [50] [51] [16] [7]
The mechanism used depends on the number of eggs previously laid.
the first explanation. Their model suggests that the kind of mechanism that parasitoids use depends on the distribution of the hosts. Parasitoids foraging for hosts with an aggregated distribution (high variability in the number of host per patch) should use incremental mechanisms, whereas those foraging for uniformly distributed hosts (low variability in the number of hosts per patch) should use decremental mechanisms. Parasitoids foraging for Poisson-distributed hosts (a mathematical assumption rather than a natural observation) should be indifferent to the number of eggs that they have laid. This model is based on the assumption that the type of host distribution is constant over generations and that there is selection for the appropriate mechanism. Nevertheless, short-term changes in the environment occur during the lifetime of individuals and they have evolved mechanisms to gather information to update their knowledge. When the number of hosts in a patch is known (e.g. when the kairomone concentration is a reliable indicator of the number of hosts in the patch), each oviposition implies a subsequent decrease in host availability. The patch becomes progressively less valuable compared with the rest of the environment and animals should use a decremental mechanism. Such a mechanism is also superior to a ‘fixed number rule’ (i.e. leave patch after x hosts have been found), because it enables a parasitoid to deal with the variation in host numbers which, although small, is always present. However, when information about host availability is unreliable (e.g. some patches are very rich, other extremely poor, but no specific cue is available), the timing of each additional oviposition reveals the quality of the patch and determines whether a parasitoid should continue to search it. In this case, an incremental mechanism would be expected. This idea was pursued both theoretically and experimentally by Driessen and Bernstein [6], who first showed that the hosts of V. canescens tend to have a uniform distribution in the field (e.g. carob fruits attacked by the moth Ectomyelois ceratoniae, a host of V. canescens, almost always contain a single host). They then showed that V. canescens obtains, at arrival in a patch, a reliable estimation of the host density by detecting the kairomone concentration. Moreover, they showed in an optimization model that for V. canescens searching individually, a http://tree.trends.com
decremental mechanism will be out-competed by an incremental one only when travel times between patches are much larger than those that are likely to occur in the field [6]. However, elaborating on this work, and using a modeling approach, Spataro (T. Spataro, PhD thesis, Lyon University, 2001) showed that when parasitoid density is high, kairomone concentration and host distribution no longer provide reliable information: host patches might have already been exploited by others and the hosts might already be parasitized. In this case, parasitoids should use an incremental mechanism. In the field, parasitoids might use cues other than kairomones to assess patch quality when the presence of competitors makes the kairomone concentration an unreliable predictor of patch quality. Marking pheromones deposited by conspecifics, contacts with parasitized hosts, or odours produced by the competitors might provide such cues. A switch from an incremental to a decremental rule occurs in the parasitoid Aphidius rhopalosiphi (Y. Outreman, PhD thesis, Rennes University, 2000). The parasitoid begins by using an incremental rule when exploiting an aggregation of wheat aphids Sitobion avenae, but switches to a decremental rule when the patch has been partly exploited. This results in the parasitoid leaving the patch long before all the hosts have been parasitized. As aphids become more and more defensive during the visit of the parasitoid, the probability that the latter becomes immobilized by a sticky substance ejected by the aphids increases. Hence, the accelerated departure decreases the mortality risk of the parasitoid [9]. Most of our knowledge about the responses of parasitoids to host encounters stems from using statistical methods that enable us to determine quantitatively the contribution of the different types of information to the instantaneous probability of leaving the patch. This became possible by the introduction [10] of the use of Cox’s proportional hazard model [11,12] into behavioural ecology, which quantifies and integrates different processes and measures how each of them contributes to the determination of patch time (Box 4). We have therefore progressed from the qualitative assessment of the influence of isolated stimuli to a more quantitative analysis, the results of which can be integrated into mechanistic or adaptive patch models [7,13]. For example, one could ask what are the optimal values of the parameters
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Box 4. Cox’s Proportional Hazards model People die, laboratory glassware breaks, parasitoids leave patches. In all these cases, something (someone) disappears. If this process happens at a constant rate, l, in deterministic terms, we would observe that the change in number over time (dN/dt ), ¼ lN, where N refers to the number (e.g. Asobara tabida females in a patch of Drosophila larvae). In probabilistic terms, mean time of disappearance is 1/l. When l is not constant but a function of time and the outcome of other intervening processes, the maths become more complicated. The proportional hazards model (and other related techniques) enables us to estimate how l is affected by different events (or covariates) and their precise timing, being for instance encounters with hosts or conspecifics. l is given as l(t,z), where z is a vector, t is the time (since the observations began, for instance). Individual zi, the covariates, might be continuous or discrete variables and might depend on time [in this case we will write zi(t )]. In 1985, Haccou and Hemerik [a] introduced into behavioural research, a statistical technique known as Proportional Hazards Analysis or Cox model, which had been used successfully in medical research to study mortality rates and to assess the effect on survival of different treatments. This technique estimates l(t,z) as (Eqn I) ! X lðt; zÞ ¼ l0 ðtÞexp bi z i ðtÞ ½Eqn I i
representing the influence of different stimuli, thus linking the causal questions to functional, evolutionary ones. The proportional hazards model has now been applied to several data sets representing a variety of parasitoid species. They include the Drosophila parasitoids Leptopilina clavipes [14] and Leptopilina heterotoma [15], V. canescens [6,7], the egg parasitoids Trichogramma brassicae and Telenomus busseolus [13,16] and the aphid parasitoid Aphidius rhopalosiphi (Y. Outreman, PhD thesis, Rennes University, 2000). Other cues affecting patch time In addition to contact kairomones and encounters with hosts, several other cues have been shown to affect patch time in parasitoids, demonstrating that foraging decisions in parasitoids are based on the assimilation of many different sorts of information. For example, the females of several parasitoid species leave a marking substance on the substrate whilst searching, and, when a female visits a patch already searched, either by herself or by a different female, she responds to the marking substance by leaving sooner in comparison with unmarked patches (i.e. encounters with the marking substance have a decremental effect) [17 – 19]. Sugimoto [20] proposed a mechanism for time allocation based on the assumption that marking pheromone concentration will increase with time in a patch. When the concentration increases above a certain threshold, the female abandons the patch. However, ovipositions would increase this leaving threshold. Decremental effects of encounters with already parasitized hosts have also been documented [13,14,16] (Y. Outreman, PhD thesis, Rennes University, 2000). This might be especially important for parasitoids searching on patches simultaneously with competitors, or on patches that have been previously visited by one or more competitors. Encounters with parasitized hosts can also http://tree.trends.com
where l0(t ) is an (unspecified) base-line rate assumed to depend only on time and is common to all possible outcomes [l0(t ) corresponds to the situation in which all covariates are set to zero] and bi are parameters. The exponential is used to assure that l(t,z) will always take positive values. For a parasitoid, t could be the time since arrival to the patch or since the last egg was laid, zi(t ) could be the number of eggs already laid, the number of conspecifics in the patch, and so on. Nonsignificant bi values correspond to processes that do not influence the outcome (e.g. patch leaving). Positive (negative) bi values will reveal processes (number of encounters with parasitized hosts, for instance) that increase (decrease) the leaving rate, so animals stay shorter (longer) times. This technique enables us to partition the influence of different processes with a minimum of a priori decisions.
Reference a Haccou, P. and Hemerik, L. (1985) The influence of larval dispersal in the cinnabar moth (Tyria jacobaea ) on predation by the red wood ant (Formica polyctena ). An analysis based on the proportional hazards model. J. Anim. Ecol. 54, 755 – 769
provide information about the current level of patch exploitation and hence about when to leave a patch. Different responses to parasitized and healthy hosts are possible only if a parasitoid can discriminate between the two. Most parasitoids have this ability, but others oviposit in each host encountered. Hosts can therefore become parasitized several times (superparasitism). The lack of host discrimination in a parasitoid can be considered as an information constraint [21]. Optimal patch time under this constraint is predicted to be shorter than without the constraint, because patches become unprofitable sooner when self-superparasitism cannot be detected and avoided. Other events, such as encounters with other parasitoids, could also result in either incremental or decremental effects on patch time, as shown for L. heterotoma [22]. Compared with females that spent the previous day alone, females that had spent the previous day with competitors stayed longer on patches and superparasitized several hosts when foraging alone the following day. This occurred because the probability of gaining offspring from a given host is proportional to the number of eggs laid on it. Thus by self-superparasitizing several hosts, the female makes the patch less attractive for competitors that find the patch after she has left and increases the probability of her producing offspring from the superparasitized hosts. In Asobara tabida, also a parasitoid of Drosophila larvae, both the quality of the previous patch and the time elapsed since the previous patch visit affects the time spent on a patch [23] in accordance with the predictions of classic optimal foraging theory [2]. The females stayed longer on the next patch after a visit to a low-quality patch and after more time had elapsed since the previous patch visit [23]. The probability of leaving a patch also increases as the number of successive patches already visited increases [16,24 – 26]. By contrast, female A. rhopalosiphi that have
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already visited a high-quality patch spend more time in the next patch (Y. Outreman, PhD thesis, Rennes University, 2000). The function of this change in behaviour remains unclear. Exposure to circumstances that indicate unfavourable environmental conditions in near future (e.g. dropping air pressure heralding a thunderstorm and low temperatures and short day length heralding the onset of winter) result in longer patch times [27,28].
Individual variation in patch leaving Internal state The internal state of a parasitoid (e.g. egg load, and lipid and carbohydrate reserves) might also provide information about future life span and affect patch time. However, few studies of parasitoid patch-leaving decisions have used a state-dependent approach [27–29] (i.e. assuming that optimal decisions will depend on the state of the animal). This approach was also used in a theoretical study of how a parasitoid should allocate its foraging time between host patches and the search of metabolic resources [30], but there are no experimental tests. The little evidence available suggests that at least in some parasitoid species, no lipogenesis occurs in the adults and that energy reserves during adult life can only be supplemented in the form of carbohydrates [31–33]. This adds a new twist to the problem by suggesting that in state-dependent models, metabolic reserves should not be represented as a single variable.
Genetic variation in patch-time allocation That patch-leaving decision rules are subject to natural selection assumes that the mechanisms are under genetic control and that there is or has been genetic variability. Indeed, genetic variation has been demonstrated in the responses of T. busseolae (a parasitoid that uses a decremental rule) to ovipositions and encounters with parasitized hosts [16]. However, this raises the question of how genetic variation is maintained in nature. The answer could be that intra- and inter-generation stochastic processes ensure that individuals experience a different environment as they sample a different subset of available patches, hence, selection within a generation would be weak and the direction of selection would fluctuate between generations.
Foraging in groups: superparasitism and time allocation Competition between adult females on a patch is usually by superparasitism, as we describe above. In a superparasitized host, the larvae of solitary parasitoids will also compete for the possession of the host. The winning larva kills the other(s). In gregarious parasitoids (i.e. competing larvae do not kill each other), superparasitism results in smaller, less-fit parasitoids emerging from that host. In spite of this, in both types of parasitoid, a female ovipositing in a host already parasitized by a competing female might still obtain offspring. Hence, superparasitism can be advantageous in circumstances where better alternatives (i.e. unparasitized hosts), are scarce. A special http://tree.trends.com
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situation occurs when competing parasitoids exploit a patch simultaneously. A female leaving before the others would leave the hosts that she has parasitized available for superparasitism. This would result in a loss of offspring unless she also stayed longer and compensated for the loss of offspring by superparasitizing herself. This results in all the females staying longer. Experimental evidence for this comes from studies of L. heterotoma [34] and A. tabida [35]. It is unknown which mechanism leads the females to stay longer. There are clear indications that odours or physical contacts could play a role [34]. Alternatively, the information about the presence of conspecific parasitoids could come from the hosts themselves. The ability to recognize hosts that are parasitized by conspecifics from hosts parasitized by the parasitoid itself has been reported in several species e.g. V. canescens [36] and Epidinocarsis lopezi [17]. Parasitoids could respond to these types of cue by changing the strength or direction of their response to host encounters. Theory about group foraging by parasitoids in depletable patches has not progressed since the early 1990s [37,38] and is one topic for which there are neither theoretical developments nor experimental tests [39]. However, it is one of the most promising avenues for future research.
Conclusion In a heterogeneous environment, animals must acquire and process information to forage efficiently because the environment changes continuously. To make adaptive decisions, animals have to compare alternatives that present themselves in a sequential manner or actual values with what they have experienced as being the mean values for the environment as a whole. We now know that parasitoids acquire and integrate information from a large variety of sources. Thus, the mechanisms involved in information acquisition and processing can be included in functional models, enabling us to predict the evolutionary consequence of the use of different mechanisms. Some of the most promising subjects for future research are the studies of state-dependent patch-leaving decisions, group foraging and the influence of experiences during previous patch visit(s). New emerging fields of research include the behavioural genetics of foraging behaviour, the optimal values of incremental and decremental responses to different stimuli and the question of to what extent parasitoids in nature are constrained by their lack of information about the spatial distribution of hosts and competitors. Current knowledge already shows that insect parasitoids are an ideal model with which to study how natural selection shapes foraging behaviour under the constraint of limited information about the environment.
Acknowledgements We thank Eric Wajnberg for stimulating discussion and Emmanuel Desouhant, Imen Djemai, Alex Kacelnik, Bart Pannebakker and two anonymous referees for suggesting improvements.
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