Ferran Garcia-Marí

Parasitoid competitive displacement and coexistence in citrus agroecosystems: linking species distribution with climate.

The introduced parasitoid wasp Aphytis melinus, the most widespread natural enemy of the California red scale (Aonidiella aurantii) and the superior competitor, has displaced the native Aphytis chrysomphali from most citrus areas of the Mediterranean basin and other citrus areas all over the world. However, our extensive survey data on the scale parasitoid populations collected in 2004-2008 show that in large citrus areas of eastern Spain both parasitoids coexist. Using field data from 179 orchards spatially divided in five citrus-producing agroecosystems, we examined the mechanisms that could explain displacement or coexistence between both Aphytis species in relation to weather conditions. The distribution and abundance of the parasitoid species are related to the mean summer and winter temperatures and relative humidity of each ecosystem. The relative proportion of A. melinus is higher during the warm months, and the abundance of A. chrysomphali increases from south to north, being higher in the cooler northern areas. Aphytis melinus has displaced A. chrysomphali from hot and dry areas, whereas regions with mild summer temperatures and moderate relative humidity present the optimal conditions for the coexistence of the two parasitoids. The more negative effects of winter temperatures on A. melinus allow the earlier use of the available host resource in late winter and spring by A. chrysomphali and the coexistence of both parasitoids in the same orchard via temporal niche partitioning. We combine previous literature on the behavior of Aphytis species in the laboratory under different temperature and humidity conditions with our field results to confirm the role of spatiotemporal weather conditions and seasonal changes in host stages on the variation of Aphytis relative abundance and parasitoid coexistence.

Recruitment of native parasitoid species by the invading leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) on citrus in Spain.

Abstract The parasitoid assemblage associated with the citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) was studied in citrus orchards in eastern Spain over a 7-yr period (1995–2001) after the leafminer’s introduction in 1994. In total, 11,587 adult native parasitoids were collected. To evaluate parasitism, 93,846 live immature stages of the citrus leafminer were observed, of which 21,460 (22.9%) were found to be parasitized. The parasitoid complex recruited around P. citrella was typical for invader hosts: lower species richness, generalized habits, idiobiont strategy, and low to moderate rates of parasitism. Two of the 10 species reared from the citrus leafminer, Pnigalio sp. and Cirrospilus brevis Zhu, LaSalle and Huang, accounted for >90% of the parasitoids. Native parasitoids moved onto the invading host rapidly, except for C. brevis, which required 3 yr to become common and widespread. In other leafminer species from plants in the vicinity of citrus orchards, the proportion of P. citrella parasitoids was higher in woody (69.7%) than in herbaceous plants (22.2%). The high population levels reached by the new pest, associated with a negative density dependence response of the parasitoids at these high population levels, suggest that the native parasitoid assemblage exerted only a limited role in regulating the population of the new host.

Effect of Mediterranean Ants (Hymenoptera: Formicidae) on California Red Scale (Hemiptera: Diaspididae) Populations in Citrus Orchards

ABSTRACT We conducted an ant-exclusion experiment in a citrus orchard to evaluate the overall impact of three ant species native in the Mediterranean, Pheidole pallidula (Nylander), Plagiolepis schmitzii Forel, and Lasius grandis (Forel), on populations of Aonidiella aurantii Maskell (California red scale). The ant-exclusion was carried out in four experimental plots from March 2007 to November 2008. Another subset of four plots, adjacent to the ant-excluded plots, was used as control. We measured scale densities and percent parasitism on fruits at harvest in 2007 and 2008. Additionally, we sampled the seasonal trend of the scale on twigs and fruits in both treatments during 2008. California red scale densities in the ant-excluded treatment began to be significantly lower than in the ant-allowed control in May (1 mo after ant activity began), and this difference increased until November. Thus, the effect of the ants on California red scale density seems to be accumulative. At harvest, scale densities on fruits were significantly lower in the ant-excluded treatment. However, percent parasitism on fruits was similar between treatments. Finally, scale densities on the fruits of the ant-allowed plots were positively correlated with the number of ants that climbed to the citrus canopy. These results suggest that increases of scale densities induced by Mediterranean ants depend on the intensity of the ant-activity on citrus canopies.

Larval cannibalism during the late developmental stages of a facultatively gregarious encyrtid endoparasitoid

1 The larvae of many gregarious parasitoid species are usually non‐aggressive when they develop in or on a host, but those of Metaphycus flavus are one of the few exceptions known. Herein we describe their aggressive behaviour and the conditions under which it occurs, using observations in which larval development and physical conflict within parasitised and superparasitised hosts were mapped daily. 2 Metaphycus flavus larvae often engaged in physical conflict that resulted in consumption of the losing larvae (= cannibalism ) in superparasitised hosts, whereas such conflict and consumption occurred rarely when a single brood developed in a host. 3 Cannibalism among M. flavus larvae only occurred after the host resources had become scarce. Typically it occurred after the sixth day of development (fourth‐instar larvae) when the larvae in a clutch had separated from their aeroscopic plate and were freed of their attachment to the hosts cuticle. 4 Female larvae in the initial clutch appeared more aggressive than male larvae when a second clutch was allocated 4 h after the first clutch. The probability of a larva being attacked and consumed by a brood mate increased as the number of larvae increased in the host. This partial tolerance might allow the members of the initial brood to defend themselves from offspring of a superparasitising female (= competitors ). Such post‐ovipositional regulation of brood size might be interpreted as high‐density intolerance among female offspring.

Guiding Classical Biological Control of an Invasive Mealybug Using Integrative Taxonomy

Delottococcus aberiae De Lotto (Hemiptera: Pseudococcidae) is a mealybug of Southern African origin that has recently been introduced into Eastern Spain. It causes severe distortions on young citrus fruits and represents a growing threat to Mediterranean citrus production. So far, biological control has proven unsatisfactory due to the absence of efficient natural enemies in Spain. Hence, the management of this pest currently relies only on chemical control. The introduction of natural enemies of D. aberiae from the native area of the pest represents a sustainable and economically viable alternative to reduce the risks linked to pesticide applications. Since biological control of mealybugs has been traditionally challenged by taxonomic misidentification, an intensive survey of Delottococcus spp. and their associated parasitoids in South Africa was required as a first step towards a classical biological control programme. Combining morphological and molecular characterization (integrative taxonomy) a total of nine mealybug species were identified in this study, including three species of Delottococcus. Different populations of D. aberiae were found on wild olive trees, in citrus orchards and on plants of Chrysanthemoides monilifera, showing intra-specific divergences according to their host plants. Interestingly, the invasive mealybug populations from Spanish orchards clustered together with the population on citrus from Limpopo Province (South Africa), sharing COI haplotypes. This result pointed to an optimum location to collect natural enemies against the invasive mealybug. A total of 14 parasitoid species were recovered from Delottococcus spp. and identified to genus and species level, by integrating morphological and molecular data. A parasitoid belonging to the genus Anagyrus, collected from D. aberiae in citrus orchards in Limpopo, is proposed here as a good biological control agent to be introduced into Spain.

The Influence of Host Fruit and Temperature on the Body Size of Adult Ceratitis capitata (Diptera: Tephritidae) Under Laboratory and Field Conditions

ABSTRACT The adult body size of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), varies in natural conditions. Body size is an important fitness indicator in the Mediterranean fruit fly; larger individuals are more competitive at mating and have a greater dispersion capacity and fertility. Both temperature during larval development and host fruit quality have been cited as possible causes for this variation. We studied the influence of host fruit and temperature during larval development on adult body size (wing area) in the laboratory, and determined body size variation in field populations of the Mediterannean fruit fly in eastern Spain. Field flies measured had two origins: 1) flies periodically collected throughout the year in field traps from 32 citrus groves, during the period 2003–2007; and 2) flies evolved from different fruit species collected between June and December in 2003 and 2004. In the lab, wing area of male and female adults varied significantly with temperature during larval development, being larger at the lowest temperature. Adult size also was significantly different depending on the host fruit in which larvae developed. The size of the flies captured at the field, either from traps or from fruits, varied seasonally showing a gradual pattern of change along the year. The largest individuals were obtained during winter and early spring and the smallest during late summer. In field conditions, the size of the adult Mediterannean fruit fly seems apparently more related with air temperature than with host fruit. The implications of this adult size pattern on the biology of C. capitata and on the application of the sterile insect technique are discussed.

Host size and spatiotemporal patterns mediate the coexistence of specialist parasitoids

Many insect parasitoids are highly specialized and thus develop on only one or a few related host species, yet some hosts are attacked by many different parasitoid species in nature. For this reason, they have been often used to examine the consequences of competitive interactions. Hosts represent limited resources for larval parasitoid development and thus one competitor usually excludes all others. Although parasitoid competition has been debated and studied over the past several decades, understanding the factors that allow for coexistence among species sharing the same host in the field remains elusive. Parasitoids may be able to coexist on the same host species if they partition host resources according to size, age, or stage, or if their dynamics vary at spatial and temporal scales. One area that has thus far received little experimental attention is if competition can alter host usage strategies in parasitoids that in the absence of competitors attack hosts of the same size in the field. Here, we test this hypothesis with two parasitoid species in the genus Aphytis, both of which are specialized on the citrus pest California red scale Aonidiella aurantii. These parasitoids prefer large scales as hosts and yet coexist in sympatry in eastern parts of Spain. Parasitoids and hosts were sampled in 12 replicated orange groves. When host exploitation by the stronger competitor, A. melinus, was high the poorer competitor, A. chrysomphali, changed its foraging strategy to prefer alternative plant substrates where it parasitized hosts of smaller size. Consequently, the inferior parasitoid species shifted both its habitat and host size as a result of competition. Our results suggest that density-dependent size-mediated asymmetric competition is the likely mechanism allowing for the coexistence of these two species, and that the use of suboptimal (small) hosts can be advantageous under conditions imposed by competition where survival in higher quality larger hosts may be greatly reduced.

Aggregation pattern, sampling plan, and intervention threshold for Pezothrips kellyanus in citrus groves

Pezothrips kellyanus (Bagnall) (Thysanoptera: Thripidae) has recently emerged as an international pest of citrus. It causes severe scarring of the fruit surface and commercial downgrading of fresh fruit production. The goals of this article were to determine the aggregation patterns of P. kellyanus on citrus, to establish an efficient sampling plan to assess their population density, and to develop an environmental economic injury level (EEIL). The study was conducted in 14 citrus groves in Valencia (Spain) during 2008 and in eight citrus groves during 2009. On each grove, population densities of thrips were monitored weekly on citrus flowers and fruitlets during the flowering and fruit setting period. Final damage was determined on developed fruits. Pezothrips kellyanus was the most abundant thrips species, with 73.5% of adults and 92.1% of larvae present, followed by Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), with 18.2 and 3.5%, respectively. First description of first instars of P. kellyanus is provided. Our results prove that thrips show clumped population distributions, with no differences in aggregation parameters between flowers and fruitlets, thrips species, larval stages, or sex of adults. Immature thrips showed a higher aggregation (Taylor’s value of b = 1.40 ± 0.06) than adults (b = 1.19 ± 0.04). Fruit damage by P. kellyanus on developed fruits was strongly correlated with percentage of fruitlets with immature P. kellyanus (r = 0.897; n = 22). Based on the percentage of fruitlets occupied by immature thrips, the economic injury levels and EEIL were calculated (using chlorpyrifos as insecticide) obtaining values of 7 and 12%, respectively. Insecticide treatments will be necessary if more than 12% of fruitlets are infested by thrips larvae. Constant precision (D = 0.25) sampling plans developed show that 200 sample units should be observed in enumerative sampling, and 310 in binomial presence–absence sampling, at population levels of immatures on fruitlets around the EEIL.

Parasitoeds (Hym.: Aphelinidae) of three scale insects (Hom.: Diaspididae) in a citrus grove in valencia, spain

The parasitoids ofAonidiella aurantii (Maskell),Lepidosaphes beckii (Newman) andParlatoria pergandii Comstock were studied in a Navel orange grove in Valencia, Spain during three years. Four species ofAphytis were identified on yellow sticky traps,Aphytis chrysomphali (Mercet),Aphytis melinus Debach,Aphytis lepidosaphes Compere andAphytis hispanicus (Mercet). No consistent annual pattern was observed in the flight of adults.A. melinus, introduced some years earlier in the grove, was found in very low numbers and showed no signs of increasing and displacingA. chrysomphali as a parasitoid ofA. aurantii. On female scales of the three species sampled at regular intervals from leaves, twigs and fruit, the mean annual rate of active parasitism was similar and ranged from 3.5% to 8%.P. pergandii males were not parasitized, inL. beckii parasitism was usually much lower in male than in female scales, and inA. aurantii it was higher in the males. Scales of the three species were less parasitized on twigs than on leaves, and so wereL. beckii on fruit. The annual trend of parasitism byAphytis on scales fluctuated without a definite pattern. Parasitism byEncarsia inquirenda (Silvestri), an endoparasitoid ofP. pergandii, was more stable throughout the year and increased steadily from year to year.RésuméLes parasitoÏdesd’Aonidiella aurantii (Maskell),Lepidosaphes beckii (Newman) etParlatoria pergandii Comstock, ont été étudiés dans un verger d’orangers de la variété Navel à Valence, Espagne, pendant trois années. Sur des pièges jaunes englués, on a identifié quatre espècesd’Aphytis: Aphytis chrysomphali (Mercet),Aphytis melinus DeBach,Aphytis lepidosaphes Compere etAphytis thispanicus (Mercet). On n’a pas observé un modèle de vol annuel évident chez les adultes.Aphytis melinus, introduit dans le verger quelques années auparavant, a été retrouvé en très petit nombre et n’a pas semblé provoquer l’augmentation ou le déplacementd’Aphytis chrysomphali comme parasitoÏded’Aonidiella aurantii. Dans les échantillonnages réalisés à intervalles réguliers sur les feuilles, branches et fruits, les femelles des trois espèces de cochenilles ont montré un taux annuel moyen de parasitisme actif entre 3, 5 et 8 %. Les mâles deParlatoria pergandii n’ont pas été parasités, le parasitisme deLepidosaphes beckii a été beaucoup plus faible chez les mâles que chez les femelles des cochenilles, et chezAonidiella aurantii il a été plus élevé chez les mâles. Les cochenilles des trois espèces ont été moins parasitées sur les branches que sur les feuilles et aussi moins sur les fruits chezLepidosaphes beckii. La tendance annuelle du parasitisme parAphytis a fluctué sans modèle défini. Le parasitisme parEncarsia inquirenda (Silvestri), un endoparasitoÏde deParlatoria pergandii, a été plus stable au cours de l’année et a augmenté progressivement chaque année.

Ants impact the energy reserves of natural enemies through the shared honeydew exploitation

1. Ants, as well as many species of parasitoids and predators, rely on sugar‐rich foods such as honeydew to fulfill their energetic needs. Thus, ants and natural enemies may interact through the shared honeydew exploitation.