Larval Cannibalism and Intraguild Predation Between the Introduced ...

COMMUNITY AND ECOSYSTEM ECOLOGY

Larval Cannibalism and Intraguild Predation Between the Introduced Green Lacewing, Chrysoperla carnea, and the Indigenous TrashCarrying Green Lacewing, Mallada desjardinsi (Neuroptera: Chrysopidae), as a Case Study of Potential Nontarget Effect Assessment ATSUSHI MOCHIZUKI,1,2 HIDESHI NAKA,1 KENJI HAMASAKI,1

AND

TAKAYUKI MITSUNAGA3

Environ. Entomol. 35(5): 1298Ð1303 (2006)

ABSTRACT To study the potential competitive risk of the introduced Chrysoperla carnea (Stephens) on the indigenous trash-carrying chrysopid Mallada desjardinsi (Nava´s), we studied the occurrence of cannibalism and intraguild predation (IGP) at different prey densities. In C. carnea, 100% cannibalism was observed in the absence of aphids. In M. desjardinsi, cannibalism was also observed, but absence of cannibalism occurred at 35% in pairs of second- ⫹ third-instar larvae and at 70% in pairs of third- ⫹ third-instar larvae. In pairs of M. desjardinsi larvae whose trash package had been artiÞcially removed, all third-instar larvae ate second-instar larvae. The trash package may play a role in the reduced mortality of younger larvae by cannibalism. IGP occurred in all pairs. In the absence of aphids, the interaction was symmetric between second-instar larvae, but asymmetric for second- versus third- and third- versus third-instar larvae, and the interaction was similar when M. desjardinsi larvae with or without trash package were paired with C. carnea larvae. When thirdinstar larvae of both species were paired, C. carnea larvae ate signiÞcantly greater numbers of M. desjardinsi larvae than vice versa. The trash package of M. desjardinsi larvae may thus not play a defensive role against IGP by C. carnea. Increasing the availability of aphids tended to decrease both cannibalism and IGP levels. Nontarget effects such as competitive displacement resulting in loss of potentially beneÞcial attributes of the indigenous M. desjardinsi by the exotic C. carnea are likely to be negligible under conditions of abundant aphids. KEY WORDS biological control, nontarget effect assessment, exotic natural enemy

Concerns have been raised that the introduction of exotic natural enemies may affect the indigenous environment (Louda et al. 2003). In Japan, green lacewings, designated as Chrysoperla carnea (Stephens), have been imported from Germany since 2001 for sale as a biopesticide for aphids. Brooks (1994) pointed out that the species is not the same as the Japanese type, which should be categorized as C. nipponensis (Okamoto). Both C. carnea and C. nipponensis belong to the carnea group, which constitutes a complex of several cryptic species and can be strictly divided into species only by their male courtship songs (Henry et al. 1993, 2001). Taki et al. (2005) recorded the courtship songs of the introduced green lacewing and conÞrmed that it was the same song pattern as the true C. carnea. The Japanese indigenous type produced a different song from C. carnea but the same as C. nipponensis as re1 National Institute for Agro-Environmental Sciences; 3-1-3 Kannondai, Tsukuba, Ibaraki 305-8604, Japan. 2 Corresponding author: Entomology Group, Dept. of Biological Safety, National Institute for Agro-Environmental Sciences, 3-1-3 Kannondai, Tsukuba, Ibaraki 305-8604, Japan (e-mail: lepi@affrc. go.jp). 3 National Agricultural Research Center, 3-1-1 Kannondai, Tsukuba, Ibaraki 305-8666, Japan.

ported by Henry and Wells (2004). There is potential for either competitive displacement or hybridization, resulting in the loss of potentially beneÞcial attributes of C. nipponensis. Mochizuki and Mitsunaga (2004) noted that interspeciÞc predation between exotic C. carnea and indigenous C. nipponensis larvae was symmetrical at the species level. InterspeciÞc hybridization between the two species was lower than conspeciÞc hybridization (Naka et al. 2005). There would thus be little nontarget impact of C. carnea on C. nipponensis in either competition or hybridization. To study the potential competitive risk of the exotic C. carnea on the other indigenous species, we chose Mallada desjardinsi (Nava´s) as another nontarget. M. desjardinsi is widely distributed in Japan and shares the same habitat as C. nipponensis. If C. carnea is established, this species will meet with M. desjardinsi in the same habitat. The larvae of M. desjardinsi carry a trash package, whereas the larvae of C. carnea are naked. This trash-carrying behavior plays an important role in protection against attack by predators (New 1969, Eisner et al. 1978, 2002). In the trashcarrying M. signata, the trash package had a major effect on reduced mortality by cannibalism (Anderson et al. 2003). We compared the propensity of canni-

0046-225X/06/1298Ð1303$04.00/0 䉷 2006 Entomological Society of America

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MOCHIZUKI ET AL.: CANNIBALISM AND IGP IN GREEN LACEWINGS

balism and intraguild predation (IGP) in C. carnea and M. desjardinsi at different prey densities under laboratory conditions and examined the role of the trash package on their competition. We also discussed the potential ecological risk of releases of the exotic C. carnea in Japan. Materials and Methods Insects. Chrysoperla carnea larvae (Kagetaro) were purchased from Arysta LifeScience (Tokyo, Japan), and M. desjardinsi were collected in Matsudo, Japan. Approximately 10 females and 10 males were maintained in a plastic cup (120 mm in diameter by 90 mm height), supplied with water and a honey-yeast diet (a mixture of water, honey, and Yeast Extract [BD Difco, Detroit, MI] as 10:10:3 mass ratio, respectively) soaked in absorbent cotton according to a modiÞed version of the method of Henry (1979). Larvae were individually reared by supplying ⬇20 mg of Entofood (frozen eggs of Ephestia kuehniella; Arysta LifeScience) every 2 d. Leaf mold was dried and sifted through 0.5-mm mesh and supplied, along with Entofood, to each larva. In the preliminary experiment, M. desjardinsi larvae carried the leaf mold well and looked identical to larvae observed in the Þeld. Second- and third-instar larvae within 24 h of molting were used in the experiments. Before the start of each experiment, larvae were starved for 24 h. All experiments were conducted in a polystyrene case (65 by 35 by 17.5 mm) under conditions of 16 L:8 D at 25⬚C. Aphids, Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae), were reared on broad bean seedlings (Vicia faba L.) under conditions of 16 L:8 D at 20⬚C. Five-day-old nymphs of similar size were used for the experiments. Cannibalism. Two conspeciÞc larvae were paired in a polystyrene case, and each pair was tested with 0, 5, 10, or 20 aphids. We paired similar-sized larvae in the same instar. Larvae with and without a trash package were tested on M. desjardinsi. Larvae without a trash package were prepared by artiÞcially removing the package from the larva using a Þne brush. The level of cannibalism in larvae without a package was only observed when no aphids were supplied. The number of larvae and aphids present and the living species and instar were recorded. Twenty replicates were done for each species and instar, respectively. Differences in the level of cannibalism in each species among aphid density were tested using a contingency table, followed by multiple comparisons with a Fisher exact probability test whose signiÞcant level was adjusted with Bonferroni correction (Sokal and Rohlf 1995). IGP. This test was conducted with a heterospeciÞc pair. The other conditions were the same as the test for cannibalism. Hypothesis of no interaction between species without aphids was analyzed with binominal test in each combination of instars. The differences in IGP levels with or without trash packages of M. desjardinsi larvae were analyzed in each combination, using contingency tables, and Fisher exact probability tests were performed on the hypothesis that the IGP levels were the same with or without the trash pack-

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ages. Differences in IGP levels as a function of aphid density in each larval combination were tested using contingency table, followed by multiple comparisons with a Fisher exact probability test whose signiÞcant level was adjusted with Bonferroni correction (Sokal and Rohlf 1995). Aphid Consumption. Each larva was put in a polystyrene case and supplied with 60 aphids. After 24 h, the number of living aphids was counted. Twenty replicates were done for each species and instar. The

Fig. 1. Cannibalism as a function of aphid density. Bars (A ⫽ cannibalism in C. carnea larvae; B ⫽ cannibalism in M. desjardinsi larvae) represent the percentage of pairs where one predator was killed. Open bars in M. desjardinsi show cannibalism between naked larvae. Percentages followed by different letters are signiÞcantly different within each species by a Fisher exact probability test whose signiÞcant level was adjusted with Bonferroni correction (P ⬍ 0.05).

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Fig. 2. IGP between two developmental stages of C. carnea and M. desjardinsi without aphids. Bars represent the percentage of pairs where one predator was killed. Open bars show the interaction between the larvae of the naked M. desjardinsi and C. carnea. *SigniÞcant asymmetry for that combination of predators (binominal test, P ⬍ 0.05).

data were analyzed with one-way analysis of variance (ANOVA), and means were separated using the Tukey-Kramer honestly signiÞcant difference (HSD) test (Sokal and Rohlf 1995). Results Cannibalism. In C. carnea, 100% cannibalism was observed in the absence of aphids within 24 h (Fig. 1A). When second- and third-instar larvae were paired, third-instar larvae always ate second-instar larvae. The frequency of cannibalism decreased with increasing number of aphids in a case (aphid density; multiple comparisons based on a Bonferroni inequality, P ⬍ 0.05). All aphids were eaten within 24 h in all cases. In M. desjardinsi, cannibalism was observed without aphids, but absence of cannibalism occurred in 10% of pairs of second- ⫹ second-instar larvae, at 35% in pairs of second- ⫹ third-instar larvae, and at 70% in pairs of third- ⫹third-instar larvae (Fig. 1B). Of pairs of naked larvae whose trash package had been removed, frequency of cannibalism was not signiÞcantly different from those of pairs of trash-carrying larvae, except for the naked second- and third-instar larval pairs, where all third-instar larvae ate second-instar larvae (multiple comparisons based on a Bonferroni inequality, P ⬍ 0.05). The frequency of cannibalism decreased with increasing aphid density (multiple comparisons based on a Bonferroni inequality, P ⬍ 0.05). If second- and third-instar larvae were paired, third-instar larvae always ate second-instar larvae. All aphids were also eaten within 24 h in all cases. IGP. In the absence of aphids, IGP occurred in all pairs. The interaction was symmetric between secondinstar larvae (binominal test, P ⫽ 0.166), but asymmetric for second- versus third- (binominal test, P ⬍ 0.001) and third- versus third-instar larvae (binominal test, P ⫽ 0.01). The interaction between trash-carrying M. desjardinsi larvae and C. carnea larvae was not signiÞcantly different from that between artiÞcially naked M. desjardinsi larvae and C. carnea larvae in any pairs (Fisher test, df ⫽ 1, P ⫽ 1.0, second instar of

M. desjardinsi ⫹ second instar of C. carnea; df ⫽ 1, P ⫽ 0.49, second instar of M. desjardinsi ⫹ third instar of C. carnea; df ⫽ 1, P ⫽ 1.0, third instar of M. desjardinsi ⫹ third instar of C. carnea; df ⫽ 1, P ⫽ 0.59, third instar of M. desjardinsi ⫹ second instar of C. carnea; Fig. 2). Of pairs at different instars, the later-instar larvae always ate the earlier-instar larvae. When two thirdinstar larvae were paired, C. carnea larvae were signiÞcantly more likely to eat M. desjardinsi larvae. Adding aphids modiÞed the IGP levels. The effect of prey density on the level of IGP varied depending on the combination of developmental stages. However, in all pairs, IGP level decreased signiÞcantly with increasing aphid density and the number of coexisting larvae increased. SigniÞcant decrease was found in the following aphid density in each pair (multiple comparisons based on a Bonferroni inequality, P ⬍ 0.05). When second-instar larvae of both species were paired, IGP level decreased signiÞcantly at an aphid density of more than Þve (Fig. 3A). When secondinstar C. carnea and third-instar M. desjardinsi larvae were paired, IGP level also decreased signiÞcantly at an aphid density of ⬎10 (Fig. 3B). The third-instar larvae of C. carnea versus second-instar larvae of M. desjardinsi pairs showed a slight decrease in IGP at an aphid density of more than Þve (Fig. 3C). When third-instar larvae of both species were paired, the IGP level also decreased signiÞcantly more than at an aphid density of 10 (Fig. 3D). Aphid Consumption. Aphid consumption within 24 h was compared among species and developmental stages. Aphid consumption (mean ⫾ SEM) in C. carnea was 29.6 ⫾ 0.9 aphids by second-instar larvae and 48.8 ⫾ 4.9 aphids by third-instar larvae, respectively. Aphid consumption (mean ⫾ SEM) in M. desjardinsi was 26.0 ⫾ 1.1 aphids by second-instar larvae and 43.8 ⫾ 0.8 aphids by third-instar larvae, respectively (Table 1). The mean number of aphids eaten by individuals signiÞcantly differed in each instar and species (Tukey-Kramer HSD test, P ⬍ 0.05), except the mean was not different between second-instar larvae of C. carnea and M. desjardinsi. The third-instar larvae

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Fig. 3. IGP as a function of aphid density. Bars (A ⫽ IGP between C. carnea L2 and M. desjardinsi L2; B ⫽ IGP between C. carnea L2 and M. desjardinsi L3; C ⫽ IGP between C. carnea L3 and M. desjardinsi L2; D ⫽ IGP between C. carnea L3 and M. desjardinsi L3) represent the percentage of pairs where one predator was killed. L2, second-instar larva; L3, third-instar larva. Percentages followed by different letters are signiÞcantly different within each combination by a Fisher exact probability test whose signiÞcant level was adjusted with Bonferroni correction (P ⬍ 0.05).

of C. carnea ate more aphids than the third-instar larvae of M. desjardinsi, and third-instar larvae always ate more aphids than second-instar larvae, irrespective of species. Discussion Cannibalism and IGP are important determinants of population dynamics and community structure (Polis et al. 1989, Polis and Holt 1992). Some researchers argue that species interactions among natural enemies through cannibalism and IGP may reduce pest suppression (Watt 1965, Force 1974, Ehler 1985, Rosenheim et al. 1995). This may lead to temporary outbreaks or ultimately to increased numbers of those Table 1.

Number aphids consumed by each larva within 24 h

Species C. carnea Second instar Third instar M. desjardinsi Second instar Third instar

N

No. aphids eaten (mean ⫾ SEM)a

20 20

29.6 ⫾ 0.9a 48.8 ⫾ 1.1c

20 20

26.0 ⫾ 1.1a 43.8 ⫾ 0.8b

a Numbers followed by different letters are signiÞcantly different by Tukey-Karmer HSD test (P ⬍ 0.05).

predators that have become less constrained by their competitors (Polis and Holt 1992). Cannibalism by C. carnea can be regarded as a mechanism for enabling survival when aphid prey is scarce (Duelli 1981, Bar and Gerling 1985). We found that the frequency of cannibalism differed according to species in the absence of aphid prey. The frequency in C. carnea was very high, but it was lower in trashcarrying M. desjardinsi larvae, except for pairs of second-instar larvae. Younger larvae are generally more vulnerable to starvation than older larvae, so that in the absence of aphids, second-instar larvae of M. desjardinsi might aggressively eat on each other, resulting in a high frequency of cannibalism. The trash package may play a role in reducing cannibalism, at least in the combination of third- and second-instar larvae of M. desjardinsi. This is supported by the result that, when the larval trash was artiÞcially removed, almost all second-instar larvae were eaten by third-instar larvae. Among third-instar larvae of M. desjardinsi, very low cannibalism was found, even in pairs of artiÞcially naked third-instar larvae. Anderson et al. (2003) reported that the trash package of M. signata was a major contributor to reduced mortality by cannibalism, and the larvae from which trash had been removed move less as they age. We also observed the same behavioral

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changes after depriving them of their trash packages. As pointed out by Smith (1926), remaining immobile may be a typical cryptic tactic by trash-carrying chrysopids if suitable trash materials are not available. In M. desjardinsi, the trash-carrying third-instar larvae were protected by their trash package, and trashremoved third-instar larvae could escape cannibalism by remaining immobile. IGP between C. carnea and trash-carrying M. desjardinsi larvae occurred in the majority of the tested combinations, most often at high levels, in the absence of extraguild prey. In general, feeding speciÞcity, body size, mobility, and aggressiveness are important factors in determining the symmetry of IGP (Polis et al. 1989, Lucas et al. 1998). The interactions among different larval instars were asymmetric between the species, which is the most common case in IGP where larger individuals kill smaller ones. Similar-sized pairs of second-instar larvae attacked each other by chance, but third-instar C. carnea larvae ate more similar-sized third-instar M. desjardinsi larvae. This is partly because third-instar C. carnea larvae were able to eat more aphids than third-instar larvae of M. desjardinsi within 24 h (Table 1). C. carnea is thus likely to be the more efÞcient consumer of aphids. The lower mobility of the third-instar M. desjardinsi larvae is another reason for their being attacked by third-instar C. carnea larvae, which move aggressively to search for food and attack anything they touch. The trash package in some genera of chrysopids plays the role of protecting against attack by predators such as ants (Eisner et al. 1978, 2002). If the trash package was artiÞcially removed from M. desjardinsi larvae, and the naked larvae were paired with C. carnea, the IGP level was not signiÞcantly different from that of pairs of trashcarrying larvae versus C. carnea. Larval shields of tortoise beetles, Charidotella bicolor (F.) and Deloyala guttata (Olivier), were not protective against predators with piercing/ sucking mouthparts, such as the hemipteran predators Podisus maculiventris (Say) (Olmstead and Denno 1993). The trash package of M. desjardinsi is not likely to provide much protection from attack by other chrysopid species, which have sickle-shaped mandibles for piercing and sucking their prey. Several authors have pointed out that cannibalism serves to stabilize predator populations when food is scarce or absent (Fox 1975). However, IGP may have a negative impact on the degree of pest suppression through its effects on the population dynamics of the predatory species (Rosenheim et al. 1995). There is a risk of competitive displacement of indigenous M. desjardinsi by exotic C. carnea at low extraguild prey densities, because C. carnea larvae signiÞcantly prey on M. desjardinsi larvae at the species level. Limited aphid availability may occur at the beginning of the season before the aphid population peaks and in the late period of aphid population decline in the Þeld. Lady beetles often seem to face food scarcity, because the number of aphids in a patch changes rapidly in both time and space (Yasuda and Shinya 1997, Osawa 2000). Obrycki et al. (1998) suspected

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that some ladybird adults collected in the Þeld, which were smaller than laboratory-reared ones, might have developed under conditions of poor food availability. In Þeld conditions, numerous predators interact with each other in aphidophagous guilds. Without prey, two erigonid spiders [Erigone atra (Blackwall) and Oedothorax apicatus (Blackwall)], a carabid beetle, Pterostichus melanarius (Illiger), and a red Þre ant, Solenopsis invicta Buren, killed C. carnea larvae (Vinson and Scarborough 1989, Dinter 1998a). Trash-carrying M. desjardinsi larvae were able to escape from attacks by the coccinellid Harmonia axyridis (Nakahira and Arakawa 2006). The superiority of C. carnea larvae over M. desjardinsi larvae may be lost by interaction with other predator species. In our experiments, both cannibalism and IGP decreased with increasing prey density. A reduction in cannibalism and IGP was observed among many predators when aphids were added (Sengonca and Frings 1985, Dinter 1998b). Lucas et al. (1998) reported, however, that reduction of IGP as a function of aphid density varied with different predator combinations. IGP between larvae of C. carnea and M. desjardinsi was signiÞcantly reduced when 10 aphids per case were added, which corresponded to less than a quarter of daily consumption by both larvae. This rapid reduction of IGP is a similar case to that between Þrst-instar larvae of C. rufilabris and Coccinella maculata, which was found when one half of daily consumption by both larvae was added, and it was explained as a behavior for avoiding the risk of encounter and competition (Lucas et al. 1998). Both C. carnea and M. desjardinsi can coexist at abundant aphid densities, and the nontarget effect of C. carnea on M. desjardinsi is likely to be negligible under conditions of abundant aphid prey. Nevertheless, careful manipulation will be necessary if using exotic C. carnea for biological control. The use of natural enemies has some environmental beneÞts such as reducing pollution by chemical pesticides. Concerning the risk posed to native ecosystems by exotic natural enemies, it would be better to use native natural enemies that represent either no risk or a predictably small level of risk. However, because production costs of native species would be very expensive in Japan, importation of the more commonly reared C. carnea is an economical solution for biological control. RiskÐ beneÞt analysis will be also necessary. Currently, the introduced C. carnea is not found naturally in the Þeld in Japan. Periodical releases in greenhouses may not result in establishment of the predator in the Þeld. Future Þeld monitoring will be needed to look at whether C. carnea will become established in Japan, and what the differences in seasonal biology and phenology might be that could impact indigenous green lacewings. Acknowledgments We thank M. Nomura and N. Haruyama at Chiba University, who provided important information. This study was supported in part by the Ministry of Environment of Japan for Research on Pollution Prevention and Control.

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MOCHIZUKI ET AL.: CANNIBALISM AND IGP IN GREEN LACEWINGS References Cited

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