Table 4.

Invertebrate organisms (insects, nematodes and molluscs) impacted by Epichloë endophytes; for other older references related to effects of Epichloë endophytes in ryegrass and tall fescue on insects, refer to Breen (1994) [252].

Organism	Impact	Alkaloid Involved	Epichloë Strain/Type	Reference
Insects
Acheta domesticus—house crickets	Toxic to nymphs	ns *	Ryegrass types	[253]
Adoryphorus coulonii—Red-headed cockchafer	Reduced (10–20%) root consumption at >1000 µg/g DM	Loline	Meadow fescue types	[254]
Agallica constricta—leaf hopper	Resistance	ns	Fescue types	[255]
Agrostis ipsilon—Black cutworm	Deterrence and toxicity	Ergovaline and/or ergine most potent, with lolines also effective	E. lolii x E. typhina hybrid from ryegrass	[256,257]
Aploneura lentisci—root aphid	Reduced survival; possible neurotoxin	Unknown (in case of AR5), and possibly epoxy janthitrems	AR37, AR5, AR6, and standard ryegrass endophyte	[258,259,260,261,262,263,264]
	Reduced root aphid numbers per plant	Possibly lolines—NFL and NAL	Fescue types	[265,266,267]
	Minimal effect	Despite having similar ergovaline levels in roots as AR5	NEA2 and NEA6 endophytes	[264]
	Increased numbers	ns	AR1 endophyte	[268]
Balanococcus poae—Pasture mealybug	Reduced survival	ns	Ryegrass types including AR1	[258,269,270,271]
	Reduced infestation	ns	Fescue types that do not express ergovaline	[272]
Blissus leucopterus hirtus—hairy chinch bug	Deterrence and toxicity to larvae and adults	ns	Fescue and ryegrass types	[273,274,275,276,277]
	No effect		Fescue types	[278]
Costelytra zealandica or C. giveni—Grass grub	Reduced root feeding and larval weight gain; a deterrent effect	Loline and increased levels due to grass grub attack	Fescue and meadow fescue types; E. uncinatum	[91,92,279,280,281,282,283,284,285,286]
Cerodontha australis—wheat sheath miner	Toxicity or deterrence to larvae, but no effect on oviposition	ns	AR47 and AR48 ryegrass strains	[287]
Crambus roman—sod webworm	Deterrent	ns	Ryegrass types (turf)	[288]
Ctenocephalides felis—cat flea larvae	Contact toxicity	NFL	Fescue types	[289]
Cyclocephala lurida—southern masked chafer	Reduced numbers	ns	Fescue types	[217]
Diuraphis noxia—Russian wheat aphid	Toxic to nymphs and adults; deterrent to adults	ns	Ryegrass and fescue types	[290,291]
Draeculacephala spp.—leaf hopper	Resistance	ns	Fescue types	[25,292]
Drosophila melanogaster—fruit fly	Toxic to adults	ns	Fescue types	[293]
Exitianus exitiosus—leaf hopper	Resistance	ns	Fescue types	[255]
Exomala orientalis	Reduced survival	ns	Fescue types	[294]
Graminella nigrifrons—leaf hopper	Resistance	ns	Fescue types	[255]
Graphania mutans—cutworm	Not a deterrent, but disrupted development	Peramine	Ryegrass types	[295]
Heteronychus arator—African black beetle	Antifeeding effect on adults	Ergopeptine alkaloids - ergotamine, ergovaline, ergocryptine	Standard ryegrass endophyte; AR22, AR12 endophytes	[260,270,280,296,297,298,299,300]
	Reduced numbers	ns	AR37 endophyte	[260]
	Deterrent, antifeeding effect on larval and adult stages	Loline	Fescue and meadow fescue types; E. uncinata	[254,301,302]
	No effect	Peramine, lolitrem B, paxilline, festuclavine, lysergol, and lysergic acid amide	Ryegrass and fescue types	[280,297,298]
Lepidogryllus spp.—mottled field cricket	Deterrent	Loline	Meadow fescue types; E. uncinatum	[303]
Listronotis bonariensis—Argentine stem weevil	Feeding deterrent for both adults and larvae; reduced oviposition	Peramine—higher concentration required to control larvae	Ryegrass types; AR1, AR5, NEA2 endophytes	[84,245,260,270,299,304,305,306,307,308,309,310,311,312,313,314,315,316,317]
	Feeding deterrent and toxin of larvae, but not adults	Lolitrem B	Ryegrass types	[315,318,319,320]
	Feeding deterrent	Paxilline	Ryegrass types	[84]
	Reduce larval damage of tillers	ns	AR37 endophyte	[260]
	Feeding deterrent and death of larvae	Loline level above 400 µg/g DM; NANL possibly more potent than NFL at moderate concentrations	Meadow fescue types	[279,321,322,323]
	Feeding deterrent	Ergovaline; ergocryptine; ergotamine	Ryegrass types	[295,324]
	No effect		Ryegrass and fescue types	[325]
Oncopeltus fasciatus—large milkweed bug	Feeding deterrent and toxic	NFL	Fescue types	[140,326]
Ostrinia nubilalis—European corn borer larvae	Toxic effects and reduced larval weight gain	NAL	Fescue types	[327]
Parapediasa teterella—bluegrass webworm	Deterrent, reduced feeding	ns	Fescue and ryegrass types	[328,329,330]
Periplaneta Americana—American cockroach	Contact toxicity	NFL	Fescue types	[289]
Phenococcus solani—mealybug	Reduced numbers	ns	Fescue types	[331]
Philobota spp.—Pasture tunnel moths	Reduced numbers	ns	AR37	[262]
Popillia japonica—Japanese beetle larvae	Contact toxicity	NFL	Fescue types	[289]
	Reduced feeding	Particularly NFL and NAL; and lesser effect of ergotamine, ergonovine, ergocryptine	Fescue types	[294,332]
	Inconsistent effects		Fescue types	[294,333]
	No effect		Fescue and ryegrass types	[334,335,336,337]
Prosapia bicincta—leaf hopper	Resistance	ns	Fescue types	[255]
Pseudococcidae—mealybugs	Reduced numbers	ns	AR37	[262]
Rhopalosiphum padi—aphid	Feeding deterrent and toxic	Loline	Fescue types	[325,326,338,339,340,341]
	Reduced numbers	ns	E. gansuense	[342]
	No effect	Ergovaline	Ryegrass and fescue types	[338]
Rhopalosiphum maidis—Corn leaf aphid	Some resistance, but less than for R. padi and S. graminum	ns	Ryegrass types; lesser impact of fescue types	[326]
Schizaphis graminum—aphid	Toxic causing reduced numbers	Loline	Fescue types; E festucae and E. uncinatum	[326,327,340]
	Feeding deterrent and toxic	Peramine	Ryegrass and fescue types	[338]
	No effect	Ergovaline
	Resistance	ns	Fescue types	[140]
Sphenphorus parvulus—Bluegrass billbug	Resistance/ toxicity to adults	ns	Ryegrass and fescue types (turf)	[288,292,343,344]
Spodoptero frugiperda—fall army worm	Reduced worm survival and liveweight gains	ns	Fescue and ryegrass types	[345,346,347,348]
		NFL, NAL	Fescue types	[327]
		Ergotamine, ergonovine, ergocryptine	Fescue types	[349]
Spodoptera eridania—southern army worm	Toxic	ns	Ryegrass types	[350]
Teleogryllus commodus—black field cricket	Deterrent	Loline	Meadow fescue types; E. uncinatum	[303]
Trigonotylus caelestialium—rice leaf bug	Resistance	Loline	Fescue types	[351]
Wiseana cervinata—Porina	Reduced survival	ns	AR37 ryegrass type	[80,192,256,352,353]
	Reduce feeding and weight gain	Paxilline		[354]
		Loline	Fescue types	[282]
Mites
Tetranychus cinnabarinus	Reduced numbers	ns	E. gansuense	[342]
Nematodes (refer to [355] Cook and Lewis 2001)
Helicotylenchus pseudorobustus—spiral nematodes	Reduced numbers	ns	Fescue types	[356]
Meloidogyne marylandi	Fewer egg masses and eggs and reduced infection	ns	Fescue types	[356,357,358]
	Reduced infection	ns, but not ergovaline	Ryegrass types	[90]
Meloidogyne nassi	Reduced galls and females	ns	Ryegrass types	[359]
Paratrichodorus minor—stubby root nematodes	Reduced numbers	ns	Fescue types	[360]
Pratylenchus scribneri—Lesion nematode	Repellent and death	NFL at high concentrations; and ergovaline	Fescue types	[356,361]
	Reduced numbers	ns	Fescue types	[362,363]
	Attractant and causes death	Ergovaline, ergotamine	Fescue types	[361]
	Repellent	Ergocryptine, ergonovine	Fescue types
	Attractant at <20 µg/m and repellent at high concentrations	NFL	Fescue types
Pratylenchus spp.	Reduced numbers in soil	ns	Ryegrass types	[364,365]
Tylenchorhynchus acutus—stunt nematodes	Reduced numbers in soil	ns	Fescue types	[362]
Molluscs
Deroceras reticulatum	Reduced feeding	Lolitrem B and possibly lolines	Used artificial diets incorporating the secondary metabolites	[366]
	No effect	Peramine
	Stimulated feeding	Ergotamine and ergovaline
	Attractant	Paxilline, lolitriol, a-paxitriol and b-paxitriol

* ns = not specified.