Ultrastructure of Symbiotic Bacteria in Normal and Antibiotic-Treated Blastocrithidia culicis and Crithidia oncopelti*

SYNOPSIS. An electron microscope study of diplosomes in Blastocrithidia culicis and bipolar bodies in Crithidia oncopelti has shown that both entities appear to be intracellular symbiotes and have a similar fine structure. They are enclosed by 2 unit membranes which are separated by a large space of very low density. The outer membrane is derived probably from the host cell. The matrix of the symbiotes is composed of dense ribosome-like particles and of areas of low density containing fine fibrillae. The particles are of the same size as ribosomes in bacteria and the fibrils have the characteristics of bacterial DNA. Thus, the lucid areas with fibrillae correspond to the nucleoids in bacteria. These observations suggest that the symbiotes are bacteria. The effect of chloramphenicol (CAP) and penicillin G (PCL) on these symbiotic bacteria was studied by culturing the host flagellates in media containing the antibiotics. The effect was analyzed at different intervals after the treatment by electron microscopy. After single treatment in the blood broth containing 0.08% (w/v) CAP, symbiotes appeared to have enlarged nucleoids, became deformed and eventually degenerated. In Grace's medium (supplemented with 10% fetal bovine serum) containing 0.6 or 2.4% (w/v) PCL, symbiotes of C. oncopelti remained unaltered, whereas some symbiotes of B. culicis became pleomorphic. Symbiotes of both species persisted after repeated transfers in PCL media and reverted to normal forms when transferred to PCL-free media. Sensitivity of symbiotes to CAP provides further evidence of their bacterial nature. The effect of PCL on the symbiotes of B. culicis suggests the presence in their cell envelopes of mucopeptide, which probably provides rigidity for maintaining the bacterial shape of the symbiotes.     

Invertebrate communities associated with macrophytes in Lake Ladoga: effects of environmental factors

Littoral invertebrate communities (meio- and macrobenthos and zooplankton) were studied in seven types of macrophyte associations commonly encountered in Lake Ladoga: in reed (Phragmites) beds on sand, soft and hard bottoms, in associations with the prevalence of Potamogeton spp., Carex spp., and Equisetum fluviatile, and in diverse vegetation stands with e.g. Polygonum amphibium, Cicuta virosa, Typha latifolia and Eleocharis acicularis. Some of the studied habitats were affected by sewage pollution, others were in comparatively undisturbed areas. Statistically significant differences between invertebrate communities in the different macrophyte associations were found. In stepwise multiple linear regression analysis the following factors were identified as determinants of abundance of aquatic invertebrates in macrophyte associations: shoot density, plant dry weight biomass, periphyton biomass, periphyton chlorophyll a, periphyton primary production, and concentrations of Sr, Mg, Ca, P, Mn, Zn, Pb and Cu. Pollution was shown to have a minor effect on the composition of littoral invertebrate communities. It is not possible to determine one single principle factor responsible for the structure and density of invertebrates in macrophyte communities.     

Identification of Two Species of Yeast-like Symbiotes in the Brown Planthopper, <Emphasis Type="Italic">Nilaparvata lugens</Emphasis>

To determine the species of the yeast-like symbionts (YLS) in the brown planthoppers (BPH), Nilaparvata lugens, YLS were first isolated and purified by ultracentrifugation from the fat bodies of BPH, and then 18S rDNA and internal transcribed spacer (ITS)–5.8S rDNA sequences of YLS were amplified with the different general primers for fungi. The results showed that the two different 18S and ITS–5.8S rDNA sequences of YLS were obtained. One 2291-bp DNA sequence, which contained 18S and ITS–5.8S rDNA, showed the high similarity to Cryptococcus and was named Cryp-Like symbiotes. Another 1248-bp DNA sequence, which contained a part of 18S and ITS–5.8S rDNA, showed the high similarity to Pichia guilliermondii and was named Pichia-Like symbiotes. It was further proved that Cryp- and Pichia-Like symbiotes existed in BPH through nested PCR with specific primers for two symbiotes and in situ hybridization analysis using digoxigenin-labeled probes. Our results showed that BPH harbored more than one species of eukaryotic YLS, which suggested that diversity of fungal endosymbiotes may be occurred in planthoppers, just like bacterial endosymbiotes.     

Cultivation,identification and quantification of one species of yeast‐like symbiotes,Candida, in the rice brown planthopper,Nilaparvata lugens

Abstract The brown planthopper (BPH), Nilaparvata lugens Stål, which is one of the most destructive pests of rice, has been confirmed to harbor yeast‐like symbiotes (YLS) in the fat body. Several morphologically different YLS have been previously isolated and cultured in vitro from BPH, but direct evidence is lacking to further clarify whether the cultured YLS were from BPH. In this study, one species of YLS was successfully cultured in vitro and simultaneously verified to exist in the fat body of BPH by sequence analysis and nested polymerase chain reaction (PCR). The cultured YLS isolate in vitro was identified as a member of the genus Candida on the basis of 18S rDNA (ribosomal DNA) and 5.8S‐ITS (internal transcribed spacer) rDNA sequence and a phylogenetic analysis of ITS sequences from yeast. Therefore, this yeast isolate was named as Candida‐like symbiotes. Candida‐like symbiotes was found to exist in fat bodies, ovaries and newly laid eggs of the BPH, but not in the heads, thoraxes and mid‐guts. In addition, the number of Candida‐like symbiotes in 1 × 10⁶ of purified YLS from BPH fat bodies was speculated to be (5.32 ± 0.22) × 10⁴ on the basis of a quantitative PCR analysis.     

Decapoda from Antipatharia, Gorgonaria and Bivalvia at the Cape Verde Islands

The shrimps Balssia gasti, Palaemonella atlantica, Periclimenes platalea, Periclimenes wirtzi, Pontonia manningi, Pontonia pinnophylax, Pontonia sp. nov., Pseudocoutierea wirtzi and the crabs Galathea intermedia and Micropisa ovata were collected from Antipatharia, Gorgonaria and Bivalvia at S?o Tiago Island, Republic of Cape Verde. Most of the associations between decapods and invertebrate hosts are reported here for the first time. This is also the first record of B. gasti and of P. wirtzi for the Cape Verde Islands. We briefly review the literature on littoral decapod crustaceans of the Cape Verde Islands. Received in revised form: 12 March 2001 Electronic Publication     

Development ofBrachymeria ovata [hymenoptera: chalcididae] in three noctuid hosts reared on artificial diet and insect-resistant and susceptible soybean genotypes

The development of the pupal parasitoidBrachymeria ovata (Say) was studied in 3 lepidopterous hosts reared on artificial diet and insect-susceptible and insectresistant soybena genotypes.Pseudoplusia includens (Walker),Anticarsia gemmatalis Hubner andHeliothis zea (Boddie) pupae from larvae reared on soybean leaves were less suitable forB. ovata development than pupae from larvae reared on artificial diet.B. ovata emergence rates, size and sometimes development period were adversely affected on plant-reared hosts. Dissection of hosts 6 days after parasitisation byB. ovata showed a higher proportion of diet-reared host pupae contained large parasitoid larvae than plant-reared hosts. Suitability differences were also detected among hosts reared on different soybean genotypes but these differences did not parallel closely the response of the lepidopterous hosts to soybean genotypes.      

Use of Alternative Food Plants Exclusively by Adult Male Froghoppers (Homoptera: Cercopidae)1

Male-specific associations of adult froghoppers (Homoptera: Cercopidae) with alternative food plant hosts is reported. Four accounts from the field and one from the literature are presented: Iphirhina quota on Bourreria costaricensis (Boraginaceae), Huaina inca on Solanaceae sp., Prosapia simulans and Prosapia sp. (near P. bicincta) on Ilex haberi (Aquifoliaceae), and Prosapia bicincta on Ilex cornuta and Ilex opaca. In three cases host use is limited to adults while in two cases use is limited to only adult males. In four cases adults feed on plants that differ taxonomically, structurally and ecologically from hosts normally utilized by all life stages. These associations are not considered aggregations per se because froghoppers are not clustered and because these associations cannot be explained by the usual criteria supporting the adaptiveness of insect aggregations. Indirect evidence suggests that these unusual hosts may be unavailable to nymphs and not sought by females. This passive lack of opportunity by nymphs and females, in tandem with an active selection/attraction by males, is a plausible explanation for the existence of male-specific hosts.     

<Emphasis Type="Italic">Galleria</Emphasis><Emphasis Type="Italic">mellonella</Emphasis> are Resistant to <Emphasis Type="Italic">Pneumocystis</Emphasis><Emphasis Type="Italic">murina</Emphasis> Infection

Studying Pneumocystis has proven to be a challenge from the perspective of propagating a significant amount of the pathogen in a facile manner. The study of several fungal pathogens has been aided by the use of invertebrate model hosts. Our efforts to infect the invertebrate larvae Galleria mellonella with Pneumocystis proved futile since P. murina neither caused disease nor was able to proliferate within G. mellonella. It did, however, show that the pathogen could be rapidly cleared from the host.     

Omikron,ein essentieller Endosymbiont von Euplotes aediculatus*†

ZUSAMMENFASSUNG. Der Süßwasserciliat Euplotes aediculatus beherbergt in seinem Cytoplasma 900–1000 stäbchenförmige Symbionten, die für seine Vermehrung essentiell zu sein scheinen. Durch Wachstum in Gegenwart von Penicillin kann Euplotes von seinen Symbionten befreit werden, es führt dies jedoch stets auch zu einem Verlust der Teilungsfähigkeit. Eine Reinfektion ist bei etwa 4% der Zellen möglich, die dann nach 4–5 Tagen sich wieder zu vermehren beginnen. Die Endosymbionten wurden sowohl lichtmikroskopisch als auch elektronenmikroskopisch untersucht. In ihrer Feinstruktur und Färbbarkeit gleichen sie, wie kappa und andere von Paramecium her bekannte “killer”-Partikel, gramnegativen Bakterien. Sie unterscheiden sich von diesen Symbionten jedoch dadurch, daß ihre DNA im Cytoplasma nicht homogen verteilt ist, sondern sich in 3–9 schon lichtmikroskopisch erkennbaren Zentren konzentriert. Die in Euplotes vorkommenden Symbionten lassen keine “killer”-Aktivität erkennen. Sie werden omikron-Partikel genannt. SYNOPSIS. The fresh water ciliate Euplotes aediculatus contains in its cytoplasm 900–1000 rod-shaped symbiotes which appear to be essential for division. Growth of Euplotes in the presence of penicillin results in loss of these symbiotes and simultaneously in a loss of the ciliate's ability to divide. Reinfection with the symbiotes can be achieved in 4% of the cells which then resume growth after a lag period of 4–5 days. The endosymbiotes have been studied by light and electron microscopy. In their fine structure and staining reaction they resemble gram-negative bacteria as do kappa and other killer particles of Paramecium. The symbiotes of Euplotes, however, are unusual in that their DNA is not distributed throughout the cytoplasm but is localized in 3–9 areas (nucleoids), which are visible even in the light microscope. No killing activity seems to be associated with the symbiotes. Following the practice of referring to those endosymbiotes by Greek letters they are here designated omikron particles.     

Variation in the structure of epifaunal invertebrate assemblages among coral hosts

The high biodiversity of coral reefs is attributable to the many invertebrate groups which live in symbiotic relationships with other reef organisms, particularly those which associate with the living coral habitat. However, few studies have examined the diversity and community structure of coral-dwelling invertebrates and how they vary among coral species. This study quantified the species richness and composition of animals associated with four common species of branching corals (Acropora nasuta, A. millepora, Pocillopora damicornis, and Seriatopora hystrix) at Lizard Island in the northern Great Barrier Reef. One hundred and seventy-eight nominal species from 12 different phyla were extracted across 50 replicate colonies of each coral host. A single coral colony, approximately 20 cm in diameter, harbored as many as 73 individuals and 24 species. There were substantial differences in invertebrate species composition among coral hosts of different families as well as genera. Twenty-seven species (15% of all taxa collected) were found on only one of the four different coral species, which may potentially indicate some level of specialization among coral hosts. The distinct assemblages on different coral species, and the presence of potential specialists, suggests invertebrate communities will be sensitive to the differential loss of branching coral species resulting from coral reef degradation.     

Foraging Ants as Scavengers on Entomopathogenic Nematode-Killed Insects

Ants were the most apparent invertebrate scavengers observed foraging on entomopathogenic nematode-killed insects (i.e., insect cadavers containing entomopathogenic nematodes and their symbiotic bacteria) in the present study. Workers of the Argentine ant,Linepithema humile(Mayr), scavenged nematode-killed insects on the surface and those buried 2 cm below the soil surface. Ant workers scavenged significantly more steinernematid-killed (60–85%) than heterorhabditid-killed (10–20%) insects. More 4-day-postinfected cadavers (hosts died within 48 h after exposure to nematodes) were scavenged than 10-day-postinfected cadavers. Ten-day-postinfected hosts contained live infective juvenile nematodes therefore ants may serve as phoretic agents. Other ant species, includingVeromessor andrei(Mayr),Pheidole vistanaForel,Formica pacificaFrancoeur, andMonomoriom ergatogynaWheeler, also scavenged nematode-killed insects. These ant species removed or destroyed about 45% of the steinernematid-killed insects. These results suggest that survival of steinernematid nematodes may be more significantly impacted by invertebrate scavengers, especially ants, than that of heterorhabditid nematodes, and placement of steinernematid-killed insects in the field for biological control may be an ineffective release strategy. Because entomopathogenic nematodes kill insects with the help of symbiotic bacteria, we tested the role of these bacterial species in deterring invertebrate scavengers by injecting bacteria (without nematodes) into insects and placing the cadavers in the field. None of the insects killed by the symbiotic bacterium,Photorhabdus luminescens(Thomas and Poinar) fromHeterorhabditis bacteriophoraPoinar, were scavanged, whereas 70% of the insects killed by the symbiotic bacterium,Xenorhabdus nematophilus(Poinar and Thomas) fromSteinernema carpocapsae(Weiser), and 90% of the insects killed byBacillus thuringiensisBerliner were scavenged by the Argentine ant. We conclude thatP. luminescensis responsible for preventing ants from foraging on heterorhabditid-killed hosts.     

Patterns of host–parasite associations in tropical lice and their passerine hosts in Cameroon

Coevolutionary processes that drive the patterns of host–parasite associations can be deduced through congruence analysis of their phylogenies. Feather lice and their avian hosts have previously been used as typical model systems for congruence analysis; however, such analyses are strongly biased toward nonpasserine hosts in the temperate zone. Further, in the Afrotropical region especially, cospeciation studies of lice and birds are entirely missing. This work supplements knowledge of host–parasite associations in lice using cospeciation analysis of feather lice (genus Myrsidea and the Brueelia complex) and their avian hosts in the tropical rainforests of Cameroon. Our analysis revealed a limited number of cospeciation events in both parasite groups. The parasite–host associations in both louse groups were predominantly shaped by host switching. Despite a general dissimilarity in phylogeny for the parasites and hosts, we found significant congruence in host–parasite distance matrices, mainly driven by associations between Brueelia lice and passerine species of the Waxbill (Estrildidae) family, and Myrsidea lice and their Bulbul (Pycnonotidae) host species. As such, our study supports the importance of complex biotic interactions in tropical environments.     

Vectored introductions of marine endosymbiotic dinoflagellates into Hawaii

Endosymbiotic dinoflagellates belonging to the genus Symbiodinium associate with a diverse range of marine invertebrate hosts and also exist free-living in the ocean. The genus is divided into eight lineages (clades A–H), which contain multiple subclade types that show geographic and host specificity. It is commonly known that free-living dinoflagellates can and have been introduced to new geographic locations, primarily through shipping ballast water. In this study we sequenced the ITS2 region of Symbiodinium found in symbiosis with the coral Acropora cytherea in the Northwestern Hawaiian Islands Marine National Monument and from shipping ballast water. Identification of an unusual symbiont in Acropora cytherea and an analysis of the distribution of this symbiont suggests an introduction to Hawaii vectored by the scyphozoan host, Cassiopea sp. Symbiodinium were also detected in shipping ballast water. This work confirms that marine invertebrate endosymbionts can be introduced to new geographic locations vectored by animal hosts or the ballast water of ships.     

Impact of parasitic mite infection on a terrestrial snail

Summary

Although parasitic infections have been shown to be critical for growth, reproduction and survival of many vertebrates, little is known about the impact of parasites on invertebrate hosts and particular on molluscs. Therefore, it is of interest how parasites may affect their invertebrate hosts and how hosts can manage the detrimental effect of infections. In the present study, the naturally widespread parasitic mite Riccardoella limacum, which has been suggested to play an important role in the ecology of the land snail Arianta arbustorum, was artificially transferred to A. arbustorum. We experimentally examined the effect of the parasite on the food consumption, shell growth, and survival of its host. Surprisingly, we found minor impacts in some traits, i.e. we found that infected and uninfected snails similarly completed their shell growth, attained sexual maturity, and allocated equal energy into their albumen glands. However, infected snails consumed less and showed a significantly higher mortality after winter than uninfected snails.     

Symbiote-Free Hemoflagellates,Blastocrithidia culicis and Crithidia oncopelti: their Liver Factor Requirement and Serologic Identity*

SYNOPSIS. Several aposymbiotic strains of Blastocrithidia culicis and Crithidia oncopelti were cultivated in Trager's chemically defined medium as well as in a blood broth, both supplemented with 0.25% (v/v) liver extract concentrate. For all such strains, the liver extract was found to serve as an essential growth factor in the defined medium and as growth promoting additive in the blood broth. The active molecules were found to be water-soluble, heat stable, dialyzable, and probably nonlipid fractions. Antisera were developed in rabbit against all the available aposymbiotic strains. An almost total cross-reactivity at very high titers was observed in reciprocal agglutination test using strains with and without the bacterial symbiotes. These results indicate that the loss of the symbiotes does not affect the antigenic identity of B. culicis and C. oncopelti.     

Co‐evolution of marine worms and their chemoautotrophic bacterial symbionts: unexpected host switches explained by ecological fitting?

Mutualistic associations of bacteria and invertebrates are widespread and encompass an enormous diversity on the side of both partners. The advantages gained from the symbiosis favour reciprocal adaptations that increase the stability of the association and can lead to codiversification of symbiont and host. While numerous examples of a strictly vertical transfer of the symbionts from parent to offspring among intracellular associations abound, little is known about the fidelity of the partners in extracellular associations, where symbionts colonize the surface or body cavity of their host. In this issue of Molecular Ecology, Zimmermann et al. ( 2016 ) investigated the evolutionary history of the symbiotic association between a monophyletic clade of sulphur‐oxidizing Gammaproteobacteria and two distantly related lineages of marine worms (nematodes and annelids). The study supports the surprising conclusion that partner fidelity does not necessarily increase with the intimacy of the association. Ectosymbionts on the cuticle of the nematodes seem to be cospeciating with their hosts, whereas endosymbionts housed in the body cavity of the annelids must have originated multiple times, probably by host switching, from ectosymbionts of sympatric nematodes. This excellent case study on the evolutionary history of invertebrate–microbe interactions supports the emerging concept that the co‐evolutionary processes shaping such mutualistic symbioses include both codiversification and ecological fitting.     

Symbiosis in the Larger Foraminiferan Sorites marginalis (with Notes on Archaias spp.)

SYNOPSIS. It was demonstrated with the aid of light and electron microscope studies that Sorites marginalis (Lamarck) harbors zooxanthellae. The hosts were scraped from Thalassia testudinum Konig growing in Key Largo Sound (Florida, U.S.A.) and immediately preserved in appropriate fixatives. Zooxanthellae were distributed unevenly throughout all the chamberlets; only a few symbiotes were found in the embryonic chambers and the inner or outer chambers, but the intermediate chambers were packed with symbiotes. The outer chambers contained many food vacuoles in addition to symbiotes. Some zooxanthellae might have been in the process of degeneration or digestion. The symbiotes were found to have a typical dinoflagellate nucleus, a single large lobate cortical chloroplast with one stalked pyrenoid, an accumulation body, and many starch granules. The nonmotile stage of the zooxanthella was similar, but perhaps not identical, to Symbiodinium microadriaticum Freudenthal from various hosts.
The foraminiferan host is heterokaryotic with hundreds of generative (small) nuclei and scores of vegetative (large) nuclei. Most of the generative nuclei were found in the embryonic apparatus and the inner chambers. Most of the vegetative nuclei were found in the inner and outer chambers.     

Influences of habitat complexity on the diversity and abundance of epiphytic invertebrates on plants

SUMMARY 1. The compound influence of habitat complexity and patch size on stream invertebrate assemblages associated with submerged macrophytes was investigated through field sampling of two natural macrophyte species with contrasting leaf morphologies (complex, Ranunculus yezoensis; simple, Sparganium emersum) and an experiment with two artificial plants with different levels of morphological complexity. 2. The artificial plant experiment was designed to separate the effects of habitat area (patch size) and habitat complexity, thus enabling a more rigorous assessment of complexity per se than in previous studies where only a single patch size was used. Simple and complex artificial plants were established with five different patch sizes corresponding to the range found in natural plants. 3. Invertebrates occurred on both complex and simple forms of natural and artificial plants at similar abundances with dipterans and ephemeropterans being predominant. Taxon richness was higher on structurally complex Ranunculus than on simple Sparganium and was similarly higher on the complex artificial plant than on the simple one, over the entire range of habitat patch sizes. Thus, architectural complexity affected the taxon richness of epiphytic invertebrates, independently of habitat scale. 4. On the natural plants there was no difference in the abundance (both number of individuals and biomass) of invertebrates between simple and complex forms, while on artificial plants more invertebrates occurred on complex than on simple forms. The amount of particulate organic matter, >225 μm (POM) and chlorophyll a showed mixed patterns on natural and artificial plants, suggesting that the availability of these resources is not an overriding proximate factor controlling invertebrate abundance on plants. The difficulty of extrapolating from experimental results involving use of artificial plants is discussed, especially when considering the relationship between habitat structure and the occurrence of epiphytic invertebrates on natural plants.     

One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of <Emphasis Type="Italic">Symbiodinium</Emphasis> types in soritid foraminifera

Recent molecular studies of symbiotic dinoflagellates (genus Symbiodinium) from a wide array of invertebrate hosts have revealed exceptional fine-scale symbiont diversity whose distribution among hosts, regions and environments exhibits significant biogeographic, ecological and evolutionary patterns. Here, similar molecular approaches using the internal transcribed spacer-2 (ITS-2) region were applied to investigate cryptic diversity in Symbiodinium inhabiting soritid foraminifera. Approximately 1,000 soritid specimens were collected and examined during a 12-month period over a 40 m depth gradient from a single reef in Guam, Micronesia. Out of 61 ITS-2 types distinguished, 46 were novel. Most types found are specific for soritid hosts, except for three types (C1, C15 and C19) that are common in metazoan hosts. The distribution of these symbionts was compared with the phylotype of their foraminiferal hosts, based on soritid small subunit ribosomal DNA sequences, and three new phylotypes of soritid hosts were identified based on these sequences. Phylogenetic analyses of 645 host-symbiont pairings revealed that most Symbiodinium types associated specifically with a particular foraminiferal host genus or species, and that the genetic diversity of these symbiont types was positively correlated with the genetic diversity found within each of the three host genera. Compared to previous molecular studies of Symbiodinium from other locations worldwide, the diversity reported here is exceptional and suggests that Micronesian coral reefs are home to a remarkably large Symbiodinium assemblage.     

Elevational contrast in predation and parasitism risk to caterpillars in a tropical rainforest

Invertebrate predators and parasitoids are among the most important natural enemies of insect herbivores. Yet, the strength of natural enemy pressure along an altitudinal gradient and interactions between the groups of natural enemies (such as predation on parasitized prey) are not well known. Various methods are used to reveal the mortality factors of herbivores. Predation pressure is usually assessed through exposure of artificial prey. However, this method cannot provide information about the attacks of parasitoids, or their eventual interactions with predators. Furthermore, artificial or dead prey might not attract predators because they do not show expected host behavior, and this method mostly cannot distinguish between predation and scavenging. For the first time in a tropical rainforest, we quantified elevational contrast in mortality factors using exposure of live caterpillars. We exposed a total of 800 live caterpillars of Talanga excelsalis moresbyensis Strand (Lepidoptera: Crambidae) on saplings of Ficus copiosa Steud. (Moraceae) at two elevations in primary tropical rain forest in Papua New Guinea (200 and 1 200 m a.s.l.). We exposed the caterpillars in two treatments: exposed to and protected from invertebrate predators and parasitoids. Disappearance of caterpillars was significantly higher in the exposed treatment. Furthermore, caterpillar disappearance was significantly higher in lowlands than in highlands (43 vs. 12%). We consider the vast majority of the disappearance to be due to predation, as migration of the caterpillars from the focal trees was not observed (except one caterpillar). This estimate of invertebrate predation rate corresponds with studies which used artificial caterpillar models. No significant difference in parasitism rate between the two elevations was observed (12 vs. 13%). The combination of the disappearance and parasitism rate patterns means that larval parasitoids face stronger pressure from invertebrate predators through higher predation of their hosts in the lowlands than in the highlands.