Eugregarines reduce susceptibility of the hide beetle, Dermestes maculatus, to apicomplexan pathogens and retard larval development

doi:10.1016/j.jip.2012.07.007

Journal of Invertebrate Pathology

Volume 111, Issue 2, October 2012, Pages 186-188

https://doi.org/10.1016/j.jip.2012.07.007 Get rights and content

Abstract

Eugregarines are abundant in a great diversity of invertebrates, and yet their relationships with their hosts are subject to controversy and confusion. We tested the effect of the eugregarine, Pyxinia crystalligera, on growth, development, and susceptibility to two Apicomplexa pathogens of the hide beetle, D. maculatus. Heavy infection with eugregarines provided partial protection from two pathogenic members of Apicomplexa, M. trogodermae and A. tribolii. Infection with P. crystalligera caused lower weight in beetle larvae, but did not significantly retard pupation or adult emergence. A. tribolii infection of Lepidoptera and M. trogodermae infection of D. maculatus are reported for the first time.

Graphical abstract

Prevalence (±SE) of infection with Mattesia trogodermae or Adelina tribolii in D. maculatus with high (>200/larva) or low (<50/larva) Pyxinia crystalligera infections.

Highlights

► Eugregarines provided protection from Mattesia trogodermae and Adelina tribolii. ► Pyxinia crystalligera caused low weight but did not retard pupation or emergence. ► First report of A. tribolii in Lepidoptera and M. trogodermae in hide beetle.

Introduction

Eugregarines are nearly ubiquitous among insects, and yet the nature of the symbiotic relationship between them and their hosts has been subject to conflicting reports and opinions. They are often referred to as parasites or pathogens, but it is not clear that they have a great negative impact on their hosts (Lange and Lord, 2011). Among eugregarines, deleterious effects on hosts have been demonstrated for aseptate species such as Ascogregarina spp. and Psychodiella spp. that infect Diptera (Er and Gokce, 2005, Lantova et al., 2011). Based on ribosomal DNA sequences, the pathogenic aseptate species are closely aligned with the neogregarines (Lantova et al., 2010, Votýpka et al., 2009), which are well known pathogens. Aside from the aseptate species, classification of eugregarines as pathogens or even parasites of insects has little empirical support. Indeed, they are frequently referred to as commensals (Lange and Lord, 2011).

We have noted apparently reduced susceptibility to challenge with Mattesia spp. of some Coleoptera with heavy eugregarine loads. The purpose of this study was to confirm that eugregarines confer protection against pathogenic Apicomplexa and to assess the effect of eugregarines on growth and development of the hide beetle, Dermestes maculatus.

Section snippets

Organisms

D. maculatus larvae were from a culture that was established in 2009 from an infestation at a western Missouri dog food plant. They were maintained on a diet of ground Purina rice and lamb dog food (Purina, Gray Summit, MO) with rolled oats. Larvae weighing from 5 to 10 mg and 14–18 days of age were used in assays. Pyxinia crystalligera (Eugregarinorida), a septate eugregarine, was present with high prevalence in the hide beetles from the time of collection. Mattesia trogodermae

Pathogen infection

Treatment with M. trogodermae resulted in a mean percentage infection of hide beetle larvae with low P. crystalligera loads that was 5.6-fold and significantly greater than the mean infection for those with high P. crystalligera loads (t = 4.2, df = 4, P = 0.013). Similarly treatment with A. tribolii resulted in a mean percentage infection that was 5.4-fold and significantly greater than the mean infection for those with high P. crystalligera loads (t = 9.5, df = 4, P < 0.01). (Fig. 1). There was no M.

Discussion

Our results demonstrate that heavy infection with gut-inhabiting eugregarines, Pyxinia crystalligera, can have both positive and negative effects on hosts. We found that infected larvae weighed significantly less than those left uninfected. More importantly, heavy infection conferred protection from orally transmitted pathogens, M. trogodermae and A. tribolii.

Most previous reports on the effects of eugregarines on their hosts investigate impact of natural levels of infection. These studies have

Acknowledgments

We are grateful to Kris Hartzer for able technical assistance and Dr. Tove Steenberg for helpful comments on a previous version of the manuscript. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.

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Morphology and molecular systematic of marine gregarines (Apicomplexa) from Southwestern Atlantic spionid polychaetes
2018, Journal of Invertebrate Pathology
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Archigregarines occur exclusively in marine habitats, infect invertebrates and have trophozoites that resemble the general morphology of the infective sporozoite stages (e.g. Schrével, 1971; Kuvardina and Simdyanov, 2002; Leander et al., 2006; Schrével et al., 2016). Eugregarines occur in marine, freshwater and terrestrial habitats infecting a great diversity of invertebrates and have intestinal trophozoites that are significantly different in morphology and behaviour from sporozoites (e.g. Lord and Omoto, 2012). Neogregarines infect insects exclusively and they have reduced trophozoite stages.
Gregarines are a common group of parasites that infect the intestines of marine invertebrates, and particularly polychaetes. Here, we describe for the first time four gregarine species that inhabit the intestines of three spionid species: Dipolydora cf. flava, Spio quadrisetosa and Boccardia proboscidea from the Patagonian coast, Argentina, using light and scanning electron microscopy and molecular phylogenetic analyses of small subunit (SSU) rDNA sequences. Even though the spionid species thrive in the same environments, our results showed a high host specificity of the gregarine species. Selenidium cf. axiferens and Polyrhabdina aff. polydorae were both identified from the intestine of D. cf. flava. The new species, Polyrhabdina madrynense sp. n. and Selenidium patagonica sp. n., were described from the intestines of S. quadrisetosa and the invasive species B. proboscidea, respectively. All specimens of D. cf. flava and S. quadrisetosa were infected by gregarines (P = 100%), recording the highest mean intensity values of infection (MI = 80; 60 respectively), in contrast to B. proboscidea (P = 60%; MI = 38). We associated this finding with the recent invasion of this host. It is expected that in the future, an increase of its population density might favour a rising intensity of this gregarine infection.
Morpho-functional characterization and esterase patterns of the midgut of Tribolium castaneum Herbst, 1797 (Coleoptera: Tenebrionidae) parasitized by Gregarina cuneata (Apicomplexa: Eugregarinidae)
2015, Micron
Citation Excerpt :
Therefore, nutritional depletion might result in size and weight reduction, as observed in the larvae of beetles Dermestes maculatus (Lord and Omoto, 2012) and Tenebrio molitor (Harry, 1967). Furthermore, the physiological processes of the host, including reproduction and development, might be compromised (Bouwma et al., 2005; Er and Gokce, 2005; Harry, 1970; Lange and Lord, 2011; Lantova et al., 2011; Lord and Omoto, 2012; Schreurs and Janovy, 2008), and eventually lead to its death (Harry, 1967; Valigurová, 2012). Therefore, infection by gregarines may represent a new strategy for biological control of pests, such as Tribolium castaneum (Coleoptera: Tenebrionidae).
Tribolium castaneum (Coleoptera: Tenebrionidae) is a common pest of stored grains and byproducts and is normally infected by Gregarina cuneata (Apicomplexa: Eugregarinidae). The life cycle of this parasite includes the sporozoite, trophozoite, gamont, gametocyte, and oocyst stages, which occur between the epithelium and lumen of the host's midgut. This study aims to describe the morphofunctional alterations in the midgut and determine the esterase patterns in T. castaneum when parasitized by gregarines. To achieve this purpose, midguts of adult insects were isolated, processed, and analysed using light and electron microscopy. We determined total protein content, amylase activity, and the expression and related activities of the esterases by using polyacrylamide gel electrophoresis (PAGE). The midgut of T. castaneum is formed by digestive, regenerative, and endocrine cells. The effects of parasitism on the digestive cells are severe, because the gregarines remain attached to these cells to absorb all the nutrients they need throughout their development. In these cells, the most common alterations observed include expansion and fragmentation of the rough endoplasmic reticulum, development of the smooth endoplasmic reticulum, changes in mitochondrial cristae, cytoplasmic vacuolization, formation of myelin structures, spherites, large intercellular spaces, autophagic vesicles, expansion of the basal labyrinth, and cytoplasmic protrusions. Deposits of glycogen granules were also observed. Amylase activity was reduced in parasitized insects. Regenerative cells were found in disorganized crypts and did not differentiate into new cells, thus, compromising the restoration of the damaged epithelium. Though few morphological alterations were observed in the endocrine cells, results suggest that the synthesis and/or release of hormones might be impaired. Nine esterases (EST-1 to 9) were identified in the midgut of T. castaneum and were expressed in varying levels in response to parasitism. Two additional isoforms of esterases were exclusively identified in the parasitized insects. The results of this study suggest that gregarines alter the morphology and physiology of the midgut. The changes may result in nutritional depletion and the impairment of other physiological processes, such as reproduction and development of the host. Thus, further studies are needed to uncover the possibility of utilizing gregarines as biological controllers of the insect pest population.
The life cycle of Gregarina cuneata in the midgut of Tribolium castaneum and the effects of parasitism on the development of insects
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Morphometric variability of clitellocephalus ophoni (eugregarinida, gregarinidae) in the intestines of Harpalus rufipes (coleoptera, carabidae)
2016, Archives of Biological Sciences
Influence of the gregarine Stenophora julipusilli (Eugregarinorida, Stenophoridae) on the trophic activity of Rossiulus kessleri (Diplopoda, Julidae)
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Journal of Invertebrate Pathology

Abstract

Graphical abstract

Highlights

Introduction

Section snippets

Organisms

Pathogen infection

Discussion

Acknowledgments

References (14)

Effect of starvation on the black carpet beetle, Attagenus megatoma, infected with the eugregarine Pyxinia frenzeli

J. Invertebr. Pathol.

Effect of Diplocystis tipulae sherlock (Eugregarinida: Apicomplexa), a coelomic gregarine pathogen of tipulids, on the larval size of Tipula paludosa meigen (Tipulidae: Diptera)

J. Invertebr. Pathol.

The life cycle and host specificity of Psychodiella sergenti n. sp. and Ps. tobbi n.sp. (Protozoa: Apicomplexa) in sand flies Phlebotomus sergenti and Ph. tobbi (Diptera: Psychodidae)

J. Invertebr. Pathol.

Parasitism in a social wasp: effect of gregarines on foraging behaviour, colony productivity, and adult mortality

Behav. Ecol. Sociobiol.

The effect of a eugregarine Gregarina polymorpha (Hammerschmidt) on the mealworm larva of Tenebrio molitor (L.) J

Protozool

Gregarina: their effect on the growth of the desert locust (Schistocerca gregaria)

Nature

The morphogenesis of Pyxinia crystalligera frenzel, a gregarine parasite of Dermestes maculatus fabr

J. Morphol.

Cited by (5)

Morphology and molecular systematic of marine gregarines (Apicomplexa) from Southwestern Atlantic spionid polychaetes

Morpho-functional characterization and esterase patterns of the midgut of Tribolium castaneum Herbst, 1797 (Coleoptera: Tenebrionidae) parasitized by Gregarina cuneata (Apicomplexa: Eugregarinidae)

The life cycle of Gregarina cuneata in the midgut of Tribolium castaneum and the effects of parasitism on the development of insects

Morphometric variability of clitellocephalus ophoni (eugregarinida, gregarinidae) in the intestines of Harpalus rufipes (coleoptera, carabidae)

Influence of the gregarine Stenophora julipusilli (Eugregarinorida, Stenophoridae) on the trophic activity of Rossiulus kessleri (Diplopoda, Julidae)

Short CommunicationEugregarines reduce susceptibility of the hide beetle, Dermestes maculatus, to apicomplexan pathogens and retard larval development

Abstract

Graphical abstract

Highlights

Introduction

Section snippets

Organisms

Pathogen infection

Discussion

Acknowledgments

J. Invertebr. Pathol.

J. Invertebr. Pathol.

J. Invertebr. Pathol.

Parasitism in a social wasp: effect of gregarines on foraging behaviour, colony productivity, and adult mortality

Behav. Ecol. Sociobiol.

The effect of a eugregarine Gregarina polymorpha (Hammerschmidt) on the mealworm larva of Tenebrio molitor (L.) J

Protozool

Gregarina: their effect on the growth of the desert locust (Schistocerca gregaria)

Nature

The morphogenesis of Pyxinia crystalligera frenzel, a gregarine parasite of Dermestes maculatus fabr

J. Morphol.

Short Communication
Eugregarines reduce susceptibility of the hide beetle, Dermestes maculatus, to apicomplexan pathogens and retard larval development