The influence of competition between foragers on ...

Behavioral Ecology Vol. 7 No. 1: 109-114

The influence of competition between foragers on clutch size decisions in an insect parasitoid with scramble larval competition Marcel E. Visser

Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK

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T almost half a century now, clutch size decisions have been studied from an adaptive point of view. Starting widi Lack (1947), the reproductive behavior of birds and mammals were explored (see review of Lessells, 1991). More recently, clutch size decisions in invertebrates have also been studied. There is a vast literature, both theoretical and experimental (see reviews of Godfray, 1987; Godfrey et al., 1991; Waage, 1986), showing that a large number of factors (like encounter rate with food patches, quality of food patches, and the egg supply of females) influence clutch size decisions in invertebrates. Many of these factors have received considerable attention from experimentalists, but one such factor, the degree of intraspecific competition, has not Intraspecific competition is, however, likely to be of importance in most natural environments, and it is therefore important to experimentally test the existing hypothesis on its effect on clutch size decisions.

Theory Species that lay clutches in or on discrete units of larval food (like plants, insects, or fruits) leave these attacked units in the environment They can therefore be reencountered by other females which might add eggs. In that case, females, when laying a clutch of eggs in an empty unit of larval food, should take into account the probability of another female laying later in the same unit The optimal clutch size in both empty and already attacked units should therefore be calculated using game theory (Maynard Smith, 1974), taking the level of intraspecific competition (the number of females ovipositing in a unit) into account. The first to consider this situation were Parker and Courtney (1984) who assumed that there are two types of females, M. E. Visser is now at the Netherlands Institute of Ecology, P.O. Box 40, 6666 ZG Heteren, The Netherlands. Received 9 January 1995; revised 18 April 1995; accepted 24 April 1995. 1045-2249/96/$5.00 O 1996 International Society for Behavioral Ecology

one always encountering empty units, the other always encountering already attacked ones. Strand and Godfray (1989) modeled females that encounter both empty and already attacked units. They predict that the clutch size laid in an empty unit decreases with increasing likelihood of another female adding eggs later on. However, as Ives (1989) pointed out, whether such a first clutch should increase or decrease with increasing levels of intraspecific competition depends on the shape of the fitness curve: the relationship between the total fitness of the offspring from that unit of resource and the number of eggs in a unit Although Ives (1989) only considered the influence of the form of the fitness curve on the effect of competition on clutch size (without specifying the form of competition between the larvae within a unit of resource), his model can be interpreted as follows. When there is scramble competition between developing individuals (resources divided roughly equally between die competing larvae), a female should lay a smaller clutch with an increasing number of females in the patch. However, when there is contest competition between developing larvae (die larvae fight or are in other direct forms of competition), the size of the first clutch should increase. This makes intuitive sense: if offspring fight for possession of the food, die chance for an individual female diat one of her offspring wins this fight increases widi clutch size. Thus, when the likelihood that another female will lay in the same food patch increases, the first female should lay a larger clutch. On the other hand, if all larvae share the food, an increasing probability of other females laying is in fact the same as reducing the amount of food available for die offspring of die first female, and thus she should lay a smaller clutch. Note that diere is thus competition on two levels: (1) competition for a unit of resource between foragers and (2) competition between larvae widiin a unit of resource. The form of the latter determines die effect of die former on clutch size decisions. In parasitoids—insects that lay Uieir eggs in or on other arthropods (hosts)—bodi forms of larval competition are found (Godfray, 1994). In solitary parasitoids, there is contest competition within a host, and only one parasitoid will

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The effect of competition between ovipositing females on their clutch size decisions is studied in animals that lay their eggs in discrete units of larval food (hosts). In such species the effect of competition depends on the form of the larval competition within such units. In insect parasitoids, there might either be contest (solitary parasitoids) or scramble competition (gregarious parasitoids) between larvae within a host For gregarious parasitoids, a decreasing clutch size with increasing competition between foragers is predicted. This prediction is tested in experiments using the parasitoid Aphaertta minuta. Parasitoids were either kept alone or in groups of four before the experiment, in which they were introduced singly in a patch containing unparasitized hosts. Animals kept together laid on average clutches of 0.74 eggs smaller than females kept alone (average clutch is 5.3), thereby confirming the prediction. Clutch size decreased with encounter number, which might be due to the adjustment of the female's estimate of the encounter rate with hosts. Finally, the results are compared with those reported for solitary parasitoids (that have scramble larval competition), for which it is predicted that the clutch size will increase with increasing levels of competition between females. Key uwrds: competition, clutch size, parasitoids, superparasitism. [Behav Ecol 7:109-114 (1996)]

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on clutch size. Also die relationship between size and fitness of females needs to be known. To diis end, parasitized hosts were collected by observing a female A. minuta searching for and ovipositing in Drosophila hydei larvae of 6 days old. Clutch size was determined by counting die movements of die abdomen by the ovipositing female. The number of bouts of vibration correlates very well widi die clutch size actually laid (observed versus found at dissection: n = 40, r2 = 0.94, p < .001; see also Vet et al., 1994; observed versus found at dissection: n = 131, Is = 0.87, p < .001), and can dierefore be used as an estimate of die clutch size laid. The parasitized hosts were reared individually in vials widi a tomato/yeast medium (500 ml tomato juice, 40 g dry yeast, 10 g agar, and die antifungal nypagine). After emergence of the offspring, die number of males and females were counted and dieir head widdi measured. From these data die relationships between clutch size and (1) the probability for an egg to survive to an adult parasitoid, (2) die size of the females emerging, and (3) die sex ratio of die offspring can be determined. Data on the relationship between size and fitness in female A. minutawere obtained by Visser (1994), and will also be used in diis study. The effect of competition on clutch size

Aim of the study There is some evidence diat solitary parasitoids lay, as predicted, larger clutches widi increasing levels of competition between parasitoid females (see Discussion). Here I will test the prediction for gregarious parasitoids diat smaller clutches are laid widi increasing levels of competition, using die parasitoid Aphaereta minuta. I will first calculate die fitness curve for this species when it attacks Drosophila hydei larvae, die host species used in die experiments. This fitness curve is then compared with die diree curves in Ives's (1989) model in order to predict die effect of competition between females on clutch size. Next an experiment is carried out in which die degree of competition is altered by keeping parasitoids eidier alone or in groups before the experiment Parasitoids are dien introduced singly onto a patch widi unparasitized hosts, and the clutch sizes laid are recorded. This setup has die advantage diat it alters the degree of competition widiout altering die rate of depletion and die amount of interaction between individuals while searching for hosts. The rationale behind it is diat females that have previously encountered conspecifics will behave as if diey are in an environment where it is likely diat odier females are going to encounter die same hosts. MATERIALS AND METHODS The parasitoid Aphaereta minuta (Nees) (Hymenoptera; Braconidae) is a gregarious, polyphagous endoparasitoid of Diptera larvae, which live in decaying plant and animal material (Evans, 1933). The host larva continues to grow after being parasitized and several adult parasitoids emerge from die host pupa. Female parasitoids search for hosts by vibrotaxis, detecting vibrations produced by die host. Once die ovipositor has been inserted into die host and die host paralyzed, die ovipositor is inserted more deeply. During oviposition, die last abdominal segments and die ovipositor sheadi undergo alternating periods of vibration and rest (Evans, 1933). The fitness curve To calculate die fitness curve, data are needed on die number, sex, and size of offspring emerging from a host, depending

The A. minuta were cultured on D. hydei Parasitized pupae were isolated (in a vial widi a layer of vermiculite) and die emerging parasitoids were mated on die day of emergence and then kept alone or in groups of four in a vial with an agar layer and honey. The wasps were used 4 days after emergence, and were kept togedier until 1 h before die experiment. As far as possible, parasitoid size was kept constant. The patches consisted of tomato juice widi agar and nypagine (200 ml tomato juice, 3 g agar, and die antifungal nypagine) and had a diameter of 8.7 cm. The hosts used were 20 D. hydei larvae of 6 days old, put in die patch 24 h before die experiment. Parasitoids were always introduced onto a patch singly and observed continuously. A full behavioral record (walking, piercing, handling host, standing still, preening, off patch, laying an egg) was made, using a Psion Organizer running The Observer (version 3.0; Noldus Information Technology, Wageningen, The Netherlands, 1990). Parasitized hosts were removed from the patch immediately after being parasitized and stored individually. There were four criteria on die basis of which die experiment was halted: (1) no hosts parasitized for 1000 s, (2) female escapes, (3) female rejects a host (ovipositor in die host for less than 5 s), and (4) female has parasitized five hosts. After die experiment die size of die parasitized hosts and of die parasitoid (head widdi) were measured and die number of eggs in die parasitoid's ovarioles counted. For each of die two treatments 12 replicates were carried out Analysis Clutch size was initially determined by counting die movements of die abdomen by die ovipositing female. In 43% of die ovipositions die movements could, however, not be seen clearly for die entire oviposition bout. For diis reason, die handling time (die time die ovipositor was inside die host), which could be measured accurately in nearly all cases, is used as a measure of clutch size. In a simple regression model handling time explained 63% of die variation in clutch size (clutch size = 1.43 + 0.0445 handling time (s), n = 58). The main explanatory variable in die analysis of handling time is die treatment (kept alone or in groups of four). Anodier variable of interest is die number of hosts previously encountered (encounter number). When searching a patch, a parasitoid will encounter hosts and may use diat information


emerge from a host. In gregarious parasitoids, there is scramble competition, and in principle all eggs can develop into new parasitoids. With increasing clutch size however, smaller parasitoids emerge. The fitness of female parasitoids usually decreases with decreasing size, because smaller parasitoids have a lower fecundity, longevity, and/or host-finding capacity (Visser, 1994). The precise shape of the fitness curve will strongly depend on this relationship between size and fitness. This is of importance because in the model of Ives (1989) a decreasing clutch size with increasing competition is only predicted when die scramble competition widiin a host is more severe than the form exp(-riV), with r > 0 and N being die number of eggs laid in a host The insect parasitoids include species with both forms of larval competition, and diis group is therefore suitable for testing predictions on the influence of intraspecific competition on clutch size. In solitary parasitoids we expect females to lay larger clutches in unparasitized hosts (i.e., lay more dian one egg although only one offspring can emerge from a host) with an increasing level of intraspecific competition, and in gregarious parasitoids we expect die females to lay smaller clutches.

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.15). The results were analyzed using generalized linear modeling techniques (Aiddn et al., 1989; Crawley, 1993), using GLIM (version 3.77; Numerical Algoridims Group, Oxford, UK, 1985). RESULTS The fitness curve In total, 45 parasitized hosts were collected. T h e probability for an egg to develop to an emerging adult decreased widi clutch size: probability of emerging = 0.99-0.10 clutch size (Aiop* = 001, r = - . 5 4 , i* = 0.29, n = 45). T h e sex ratio (proportion males) did not significandy decrease widi clutch size (^.lop,. = .35, n = 45). This is because from small clutches (two to diree eggs) often only females emerged. The size of emerging females (head widdi) decreased widi clutch size:

Mean time spent handling a host (bars indicate SE, plotted in only one direction to avoid overlap) versus encounter number for female A. minuta kept in groups of four (open symbols) or kept alone (closed symbols) before the experiment The lines connect the fitted values (see Table 1).

head widdi (mm) = 0.60-0.02 clutch size ( / ^ = .004, r = — .48, J2 = .23, n = 35). In order to calculate die fitness curve, die relationship between size of a female and her fitness needs to be known. I used die data in Visser (1994) on die sizedependent constraints in longevity, fecundity and searching efficiency in A. minuta. These are combined into one fitness measure, using a dynamic programming model (see Visser, 1994, for details). This model was used by Visser (1994) for a different host species, so I recalculated this relationship widi D. hydei as a host species: fitness 9 = 0.5 — 2.2 head widdi 9 + 2.7 (head widdi 9) 2 . The fitness curve can now be calculated using die equation: fitness clutch = clutch size X probability of emerging X fitness 2 (head width 9) (The sex ratio of die emerging parasitoids is left out because diere was no relationship between sex ratio and clutch size.) This fitness curve is plotted in Figure 1 togedier with die diree curves from Ives's (1989) figure. It is clear diat die fitness curve falls below die larval-competition curve for which Ives's model predicts no change in clutch size widi increasing competition between foragers (fitness = (ie"'", widi u. > 0, r > 0, and N = clutch size). Thus, for A. minuta attacking D. hydei, clutch size is predicted to decrease widi increasing competition between female parasitoids. The effect of competition on clutch size The degree of intraspecific competition, as altered by keeping parasitoids eidier alone or in groups of four before the experiment, was found to have an effect on clutch size (Table 1 and Figure 2) in die predicted direction. Females kept togedier before die experiment handled hosts on average 16.6 s shorter dian females kept alone, which corresponds widi a decrease in clutch size of 0.74 eggs (using die equation, clutch size = 1.43 + 0.0445 handling time). The encounter number also had a significant effect; clutch size decreased over die first diree encounters. There is no


Clutch size

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Table 1 Generalized linear model on handling time (n = 109), which is highly correlated to clutch size

Null model Residual Treatment Encounter number6

Change in deviance

df

Change in

P

102,252 78,560 7443 16,645

108 105 1 2