Oecologia (Berl.) 35, 55-89 (1978) Biochemical and Evolutionary Aspects of Arthropod Predation on Ferns Michael J. Balickl, David G. Furthz, and Gillian Cooper-Driver3 * ' Botanical Museum of Harvard University, Oxford Street, Cambridge, MA 02138, USA ' Department of Biology. Yale University, New Haven, CT 06520, USA ' Jhpartment of Biological Sciences, Boston University, 2 Cummington St., Boston, MA 02215, USA Summary. The widely held assumption that very few arthropods feed on ferns was questioned following field observations of arthropod damage on ferns in the state of Veracruz, Mexico. The extent and type of damage was recorded and it was found that in a measured locality, ferns were no less attacked than the angiospermous flora. As chemistry and arthropod host relationships have been shown to be so closely intertwined, plants collected in the field were analysed for both condensed tannins and cyanoge- nic glycosides, compounds known to be effedtive deterrents in temperate climates. Although all ferns tested contained tannins these did not appear to inhibit predation. Cyanogenic glycosides were present in only 3% of the fern species analysed, and it is, therefork unlikely that they play a significant role as defensive compounds in the ferns examined. A literature search revealed a large number of ferns cited as being arthro- pod hosts. Approximately 420 named species of arthropods have been recorded, the majority of which are from the orders Coleoptera, Hymen- optera,. Lepidoptera, and Hemiptera. Both evolutionary primitive (sawflies) and advanced (moths) arthropods are reported to be present on ferns suggest- ing possible coevolution of arthropods and ferns both before and after the radiation of angiosperms. I. Introduction It is assumed that ferns generally are not eaten by herbivorous insects (Soo Hoo and Fraenkel, 1964; Eastopp 1973; Southwood, 1973). Indeed in their cl'assical paper on the co-evolution of bufferflies and plants Ehrlich and Raven (1964) state "In fact, very few insects feed on ferns at 'all, a most surprising and as yet unexplained fact with no evident chemical or mechanical basis ". 'Some ferns have toxic effects on both invertebrates (Carlisle and Ellis, 1968) * To whom offprint requests should be sent
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Biochemical and Evolutionary Aspects of Arthropod ... · climates. Although all ferns tested contained tannins these did not appear to inhibit predation. Cyanogenic glycosides were
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Oecologia (Berl.) 35, 55-89 (1978)
Biochemical and Evolutionary Aspects of Arthropod Predation on Ferns
Michael J. Balickl, David G. Furthz, and Gillian Cooper-Driver3 * ' Botanical Museum of Harvard University, Oxford Street, Cambridge, MA 02138, USA ' Department of Biology. Yale University, New Haven, CT 06520, USA ' Jhpartment of Biological Sciences, Boston University, 2 Cummington St., Boston, MA 02215, USA
Summary. The widely held assumption that very few arthropods feed on ferns was questioned following field observations of arthropod damage on ferns in the state of Veracruz, Mexico. The extent and type of damage was recorded and it was found that in a measured locality, ferns were no less attacked than the angiospermous flora. As chemistry and arthropod host relationships have been shown to be so closely intertwined, plants collected in the field were analysed for both condensed tannins and cyanoge- nic glycosides, compounds known to be effedtive deterrents in temperate climates. Although all ferns tested contained tannins these did not appear to inhibit predation. Cyanogenic glycosides were present in only 3% of the fern species analysed, and it is, therefork unlikely that they play a significant role as defensive compounds in the ferns examined.
A literature search revealed a large number of ferns cited as being arthro- pod hosts. Approximately 420 named species of arthropods have been recorded, the majority of which are from the orders Coleoptera, Hymen- optera,. Lepidoptera, and Hemiptera. Both evolutionary primitive (sawflies) and advanced (moths) arthropods are reported to be present on ferns suggest- ing possible coevolution of arthropods and ferns both before and after the radiation of angiosperms.
I. Introduction
It is assumed that ferns generally are not eaten by herbivorous insects (Soo Hoo and Fraenkel, 1964; Eastopp 1973; Southwood, 1973). Indeed in their cl'assical paper on the co-evolution of bufferflies and plants Ehrlich and Raven (1964) state "In fact, very few insects feed on ferns at 'all, a most surprising and as yet unexplained fact with no evident chemical or mechanical basis ". 'Some ferns have toxic effects on both invertebrates (Carlisle and Ellis, 1968) * To whom offprint requests should be sent
M.J. Balick et a].
as well as vertebrates (I.A. Evans, 1976; W.C. Evans, 1976), but as have generally managed to exploit most other toxic plants, why is it that they have been reported to avoid ferns?
During field studies on the biology of ferns in the state of Veracruz, Mexico (March-April, 1976) it was noticed that many of the ferns showed a considerable amount of damage which was apparently due to arthropod feeding. It appeared, therefore, that entomologists and field ecologists may have either over-looked or ignored ferns as possible host plants for insect herbivores. Since earlier work had shown that two groups of secondary plant compounds, the tannins and cyanogenic glycosides (Cooper-Driver et al., 1977), are probably important in determining the extent of herbivore attack on a given fern species, the original observations were followed up with estimations of the amounts of these com- pounds in selected fern species. We also carried out an extensive literature search revealing a large number of references to ferns being used as host plants by arthropods, although it must be stressed that these records are not always clear as to whether the host plant was providing shelter or food. Few of these records relate to tropical flora and fauna, surprisingly in that insects are much more diverse in the tropics than elsewhere and doubtless constitute the major class of herbivorous animals (Janzen, 1975).
From these preliminary observations on the degree and type of damage to Mexican ferns and from the records in the literature, it is concluded that the widely held assumption that very few arthropods feed on ferns, is not well founded. The chemical studies showed that while both tannins and cyanoge- nic glycosides were present in the ferns examined, their role as efficient feeding deterrents may not be as great as in other plant phyla (Swain, 1977), or as in temperate fern species (Cooper-Driver, 1976; Lawton, 1976). These findings are used to discuss the way in which ferns, during the course of evolution, have developed defensive strategies and in fact have co-evolved with their arthro- pod predators.
11. Materials and Methods
I . Field Collection
All field studies and collections were made in the state of Veracruz, Mexico near Jalopa in areas around Puente National, Misantla, Las Vigas and Perote, during March-April 1976. A total of six ecologically diverse sites were visited and every species of fern in the area was examined for insects or visible indications of damage due to insect feeding. Many of the specimans were collected, pressed, dried and examined in the laboratory. To determine the relative amount of damage to ferns and other plants, an "ecological plot", 2 by 4 m was laid out in a Liquidambar forest site at 1350 m altitude near Las Vigas. The location of the individual plants was recorded and a survey for insect damage made. Representative samples of each plant were pressed and dried and a rough estimate of the amount of damage obtained by photocopying the plants, cutting out the outline on the copy and weighing it (A, "intact plant") then removing from the copy the (white) area plainly showing damage (B) and weighing this. The percentage damage was then B/A x 100.
2. Chemical In~stigations
Chemical tests were carried out using both fresh and dried material. The presence of a cyanogenic glycoside was determined using the method of Eyjolfsson (1970). Fresh frond samples in the field
Biochemical and Evolutionary Aspects of Arthropod Predation on Ferns
were tested for the production of HCN by treating the material (ca. 1.5 g of terminal pinnae) with 2-3 drops of toluene in a sealed tube with a filter paper strip, which had been pre-treated with sodium picrate solution, suspended from the stopper and leaving the tube at room temperature for 24 h. Any change in the color of the papers from yellow to brown that was observed indicated that HCN had been released.
Estimation for condensed tannins was carried out in the laboratory on dried specimans. The plant material was extracted twice with 80% boiling methanol and the extracts combined. Equal volumes of the extract and 5% conc. HCI in n-butanol were heated at 100" C for 40 min and the absorbtivity read at 530 nm (modification of Swain and Hillis, 1959). Quebracho tannin was used as the standard.
3. Literature Search
This was carried out using abstract literature from Biological Abstracts, Review of Applied entomol- ogy and Bibliography of Agriculture from 1930 up to the present time. In addition, the entomological libraries of the Connecticut Agricultural Experimental Station, Yale University and Harvard (Museum Comparative Zoology) were xanned for host plant data in taxonomic monogaphs or faunal surveys.
1. Survey for Arthropod Damage
Of the 137 fern species collected in the Veracruz area of Mexico, insect damage was noted in a total of 26 or approximately 19% of the total fern flora observed. Species for which damage was recorded are given in Table 1. The damage ranged from slight to that which appeared to be severe enough to have affected . the photosynthetic and reproductive capacity of the plant. Despite signs of considerable insect damage to the ferns in this tropical Mexican locality there : were very few arthropods actually found on the ferns at the time of collecting. This may be due to a predominance of nocturnal feeding, arthropod seasonality in the Mexican populations, collecting techniques, or some other factors. Subse- quent careful examination of pressed ferns from this locality revealed several different types of apparent arthropod damage. We have speculated, with each damage-type, which insect order might have caused the particular damage. These are as follows: a) small crescent notching of pinnules either at apex, base, or bases of several adjacent pinnules - Coleoptera (Curculionidae) (Fig. 1) ; b) large notching of pinnae-Lepidoptera, possibly Orthoptera (Figs. 2 and 5); c) skeletonization of upper surface of pinnule between the veins- Lepidoptera, Coleoptera (Fig. 3); d) shot-hole (upper surface), often concentrated but not always spherical -possibly Hemiptera (Homoptera) (Fig. 4); e) complete or par- tial elimination of several or many pinnules on one or both sides of the rachis- Lepidoptera (Fig. 6). Several fern species displayed fungal or viral damage and it may be that these pathogens are transmitted by arthropod vectors, i.e. aphids ' or leafhoppers, as is known to occur in other plants (Wood, 1967).
The 8 square meter plot in the Liquidambar forest contained 3 species of ferns and 6 other flowering plant genera. The average percentage dafnage to the leaves of several selected individuals of these different taxa is recorded in Table 2. From these results it is apparent that ferns were preferred as a
M.J. Balick et al.
Table 1. Fern species collected in Veracruz, Mexico on which arthropod damage was recorded, most of which were subsequently analysed for condensed tannins
Taxa % condensed Proposed type tannin of arthropod mg/g dry weight damage
Adiantum fenerum Sw. 8.40 Anemin adiantifolia (L.) Sw. 7.80 Asplenium momnfhes L. 0.90 Blechnum varians (Fourn.) C. Chr. 5.10 Ctenifis subincisa (Willd.) Ching a - Cyrtomium juglandfolium ( H + B ) Moore - Dicksonia ghiesbreghtii Maxon - Dryopteris parallelogramma (Kze.) Alston 5.40 Eluphoglosum latifoium (Sw.) J. Sm. 12.30 Hypolepis reprms (L.) Presl. 0.14 Lygodium mexicanwn Presl. 0.30 Polypodium aureum L. 0.60 Polypodium Ianceolarum L. - Polypodum loricewn L. 0.60 Polypodium pectimtum L. - Polypodium plebejium Schlect. +Cham. 5.10 Polypodium puberulum Schlect. + Cham. 0.60 Polystichum muricatum (L.) Fee 16.00 Pteridium aquilinum (L.) Kuhn var. caudatum (L.) Sadeebeck 8.50 Pteris dejlexa Link 1.80 Tectaria heraclefolia (Wilid.) Underw. 8.10 Thelypteris kunaii (Desv.) Morton 3.70 , Thelypteris cheilanthoides 3.90 Thelypteris normalis (C. Chr.) Moxley - Thelypteris tetragona Sw. 5.0 , Woodwardia martinezii Maxon. 9.0
C
a d a, b a a a a, b, c, e a, b a, d, e a a b . a, b a, b a, b, e a, e a, d a + fungal damage e a, d a, b a a, b b e
These plants were not analysed for tannins
food source, or at least showed a higher degree of predation, than the ac- companying angiosperms in this particular plot.
2. Chemical Investigations
Out of the 100 fern species tested for cyanogenesis only 3 gave a positive result: Cheilanthes intramarginalis, C. marginata and Notholaena aurea. Two other Cheilanthes species had previously been found to be cyanogenic (Harper et al., 1976).
All ferns examined in the survey had the ability to produce condensed tannins although theactual amounts of tannins in tlie species analysed varied from 0.3%-16% mgms per gram dry weight (Table 1). Levels of tannins in the plant taxa of the ecological plot are given in Table 2. There was no apparent correlation between the percentage of damage to the leaf of frond material by feeding arthropods and the percentage of tannins per gram dry weight of plant material.
Figs. 1-6. Illustrations of presumed insect dal Fig. 1. Hypolepis repans (L.) Presl Fig. 2. Polypodium Ianceolarum L Fig. 3. Adianrum renerum Sw Fig. 4. Asplenium monanthes L. Fig. 5. Thelypteris rerragona Sw.
Fig. 6. Reris dejlexa Link
I to fern species
M.J. Balick et al.
Table2 Degree of arthropod damage recorded on the leaves of plants in a 8sq. meter plot in a Liquidambar forest, Veracruz, Mexico. These were subsequently analysed for condensed tannins
Taxa % estimated damage to % condensed tannin leaf or frond area by mg/g dry weight feeding arthropods
Five populations of different fern species were selected at random and samples of eaten and uneaten fronds were collected for each species within the same population. The eaten and uneaten fronds were then analysed for their tannin content. Results are given in Table 3. There was no over-all correla- tion between % tannins in eaten and uneaten fronds, although there was a tendency in three of the species, for the levels to be slightly higher in uneaten than in eaten material.
3. Literature Data
The results of the literature survey are tabulated in Appendix 1. The data are alphabetically arranged (by Orders, Families, Genera and Species) according to the nomenclature of Brues et al. (1954). In addition to the fern-arthropod
Biochemical and Evolutionary Aspects of Arthropod Predation on Ferns
records, ecological information has been recorded wherever possible after the arthropod name. Those insect species known to feed on several non-fern hosts are indicated as being polyphagous (P), whereas those with only a few non-fern hosts as oligophagous (0). The mode of feeding is also indicated when known, i.e. sporangia feeders (s), gall-formers (g), root-stock or rhizome feeders (r), miners or borers (m), and decaying frond feeders (d). The remainder are assumed to be primary frond feeders. Wherever a record is questionable either by the au- thor's admission, or because it is a secondary predator or parasite (or otherwise), it is cited as a fern associate (assoc.) which is indicated after the specific arthro- pod binomial. For all fern-arthropod relationships listed, the locality and au- thor's name with a reference are given for more detailed reading. It must be stressed that Appendix 1 contains only recorded data and it is inevitable that there will be some cases of misidentification or synonomy of arthropods and their fern hosts, particularily in the case of older records. In addition this table does not claim to give a complete list of all insects recorded as being present on ferns; nevertheless this is the most comprehensive treatment that has been produced up to the present .time and hopefully will serve as the basis for further compilations.
From an analysis of our data there appears to be a more or less even distribution of types of feeders: root feeders (3.3%), spore feeders (2.4%), miners or borers (5.9%), gall formers (4.3%) and decay feeders (4.0%). 73% are restricted to ferns whereas 27% are polyphagous or oligophagous. This indicates that most fern feeders must have had to specialize in order to have co-evolved with the chemistry of ferns.
IV. Discussion
No previous paper has presented evidence of arthropod-fern associations on such a broad scale (Appendix 1). The only extensive listing of fern insect pests is by Docters Van Leeuween (1938) in Verdoorn's Manual of Pteridology. Other surveys have been restricted to regions such as Hawaii (Swezey, 1922), North American fern aphids (Robinson, 1966), Western Hemisphere fern mites (De Leon, 1966), or to insects present on a particular fern; Simmonds (1967), Wiec- zorek (1973), Lawton (1976) and Kirk (1977) all have recorded insects present on bracken, Pteridium aquilinum. Hoshizaki (1975) provides a common name list of fern pests; however, these are primarily at the ordinal level.
Approximately 420 species of arthropods have been recorded from fern hosts in Appendix 1, together with 44 fern associates and several references to unnamed insect species. It is not certain as to exactly which insects were actually feeding on the ferns rather than using them as a refuge or a transient resource; neither do we know whether the arthropods and ferns have been correctly identified in the older records. The list cannot be truly representative for all fern genera since over 22% of the records refer to the economically important fern bracken, the most widely distributed and probably the best known of all pteridophytes (Perring and Gardiner, 1976). It might be expected that there would be more data on arthropods feeding on ferns in the tropics
M.J. Balick et al.
than in the temperate zones especially since pteridophytes are more abundant and more diverse in tropical areas.
Nevertheless from this compilation several inferences can be made. Of the 420 arthropod species recorded on ferns, 59% constitute the more advanced Holometabola: the largest groups in number of species, are in the orders Co- leoptera, Hymenoptera and Lepidoptera.
The Coleoptera exhibit a scattered diversity of fern feeders and the weevils, the most diverse family of insects, are probably quite widely associated with ferns all around the world, especially in the tropics. Zimmerman (1957) lists many Miocalles weevils from Oceania and demonstrates the high affinity of these insects for ferns.
The ferns collected in Mexico also apparently showed a significant amount of weevil damage (a, Table 1). Vanin (1976) considers the Gondwanian belid weevils to be primitive not only because of their morphology but also their phytophagy of ferns and gymnosperms.
There is a predominance of primitive sawflies within fern feeding Hymen- optera. Sawflies form a dominant group of the restricted fern feeding commu- nity throughout the Holartic region. Lawton (1976) found only one of the 43 "common" British seed plants had more sawflies than bracken. In contrast to most other groups of arthropods, it seems quite likely that these wasps may have co-evolved with ferns before angiosperm dominance in the late Cre- taceous.
Among the Lepidoptera, the Noctuidae are the most numerous fern feeders with the genera Callopstria and Papaipema containing many specialist fern feed- ing species. Lepidoptera are considered to be the most advanced of holometabo- lous insects, known since the Cretaceous (Ehrlich and Raven, 1964; Mackay, 1970). Although Ehrlich and Raven have proposed that Lepyoptera diversity has elaborated along with the dicotyledons and that those inembers feeding on non-dicots show secondary adaptation and are probably more advanced, our records show that it is the primitive Lepidoptera, moths such as the Hepia- lidae rather than butterflies and higher moths, that are recorded as being present on ferns.
The hemimetabolous Hemiptera (especially the Hornoptera) are also appar- ently important fern feeders. Aphids (Aphididae) are able to utilize a large number of divergent species as host plants suggesting that they may be able to avoid some of the chemical defenses of most plants due to their specialized piercing-sucking method of feeding. Aphids may thus not have to contend with plant toxins in high concentrations since such compounds are usually more or less absent from the phloem transport stream or occur there in much lower concentrations than in the rest of the plant (Van Emden, 1972). Eastop (1973) records 29 species of aphids, from several different aphid groups, restricted
' to ferns. He also notes that aphids, unlike most arthropods, are' less abundant and more polyphagous in the tropics, which perhaps explains why we did not find much evidence of aphid predation in our Mexican samples (d, Table 1).
The oldest arthropod order recorded on extant ferns is the Orthoptera which has fossil representatives in the Carboniferous (Smart and Hughes, 1973), how- ever, there are very few recorded on today's ferns. Other arthropod orders,
Biochemical and Evolutionary Aspects of Arthropod Predation on Ferns
with more recent fossil history, i.e. Diptera (early Mesozoic) and Thysanoptera (Permian) also contain restricted fern feeders.
The wide scattering of recorded fern arthropod hosts does not reveal an obvious association with primitive or more advanced arthropods. Plants have apparently responded to insect attack in various ways since they became estab- lished on land (Kevan et al., 1975; Swain, 1978), and thus insects and plants must be viewed as two co-evolving, competing and often mutually dependent biochemical systems (Ehrlich and Raven, 1964). In any given ecosystem the fates of the various guilds of herbivorous insects and plants are chemically intertwined (Whittaker and Feeny, 1971 ; Gilbert and Raven, 1975; Swain, 1977). Fossils of arthropods found in the early Devonian were arachnids with mouth- parts which could pierce plant stems and spores, and in this period many insects fed on spores, spore protoplasts and plant sap. The evolution of winged insects in the late Devonian was accompanied by an. increase in arborescent forms of plants and in the complexity of certain groups of secondary plant compounds. The ability to produce chemically more resistant spores and cell walls, to synthesize lignin and general purpose antibiotics and feeding deterrents was as important in the evolution of plants as changes in their anatomy and morphology (Swain, 1978).
The condensed tannins are one of the most important of all plant chemical defenses; not only are they potent anti-fungal, anti-bacterial and even antiviral agents but they bestow on plants, that have the ability to synthesize them, a powerful feeding deterrent to many herbivores (Swain, 1977, 1978). All ferns, with the exception of the Ophioglossales, which have a comparatively recent fossil history, have the ability to synthesize tannins. As there is a higher propor-: tion of species containing proanthocyanidins in the Filicales than in the lower tracheophytes, gymnosperms, or angiosperms, it is likely that proanthocyanidins ' arose as the first soluble anti-fungal and insect feeding deterrent but were later reinforced or replaced in angiosperms by ellagitannins or by more selective terpenoid or other feeding deterrents. Although correlations have been reported between amounts of tannins and degree of arthropod feeding inhibition (Feeny, 1970; Lawton, 1976; Rhoades and Cates, 1976; Cooper-Driver et al., 1977); the data were from plants growing in temperate climates. Results also vary according to the time of year, tannin levels usually being higher in deciduous temperate plants towards the end of the growing season. As the tannin levels rise, the extractable protein content drops decreasing the nutritional value of the plant as a source of food. In the tropics, however, with perhaps more rapid co-evolution of both herbivore and host, it may be that insects have developed a higher degree of tolerance to tannins which may not be such an effective means of defense. This may explain why many of the ferns with high tannin levels were still subject to insect attack.
Ferns do however possess a number of other defensive compounds (Swain and Cooper-Driver, 1973). The ecdysones or insect molting hormones are found inmany ferns. It has been assumed that the role of phytoecdysones is to induce metamorphosis in arthropods thus causing lethal anomolous development (He- rout, 1970). However laboratory experiments using a variety of insects i.e. Musca, Cynthia, Hyalophora, Manduca, Trichoplusia, Tribolium, Blatella, Thermobia and
M.J. Balick et al.
Schistocerca (Robbins et al., 1968; Williams, 1970; Hendrix, 1977) have not been able to substantiate the effects of ecdysones under natural conditions using whole plants. The phytoecdysones occur more commonly in those species of ferns which are considered to be advanced e.g. Polypodium and Pteridium and which, by and large, also possess a wider range of other potentially deterrent toxic compounds such as the bitter sesquiterpenoid lactones and cyanogenic glycosides.
The cyanogenic glycosides break down under the action of B-glucosidase to produce hydrogen cyanide known to be toxic to many herbivores (Jones, 1973; Cooper-Driver and Swain, 1976). Although these compounds are not very common in ferns, occurring in approximately 3% of species (Harper et al., 1975), nevertheless they are effective feeding inhibitors. Of the 2 Cheilanthes and 1 Notholaena species that were found to be positive for HCN production, in this study; none of these had been attacked by insects. As hydrogen cyanide production varies with age, season and a number of environmental factors,
. much more work still needs to be done before we can ascertain the importance of this particular group of chemicals to the total ecosystem.
V. Conclusion
It is apparent from the data presented that many more arthropods are in fact present on ferns, than has previously been thought, and that many have over- come the fern's chemical defense systems to utilize them as food, particular~ in the tropics where coevolution proceeds at a more rapid rate.
A study of such interactions with ferns provides a good system for examining theories of coevolution since they are at the juQction of primitive vascular plants and the more specialized seed-bearing plants, and have a long fossil record from the late Devonian (Banks, 1972).
A systematic search is needed to examine the species of insects which feed on different taxa of ferns and in what frequency; to determine seasonality of feeding correlated with changes in plant and insect chemistry, to analyse secondary plant compounds present in temperate and tropical fern species, and finally controlled feeding tests are needed to determine insect preference when a selection of suitable hosts is offered. It is hoped that this paper will stimulate direct field observations in both temperate and tropical areas. Data from all such observations could begin to shed new light on the important biological phenomenon of coevolution.
Acknowledgemenrs. We thank Drs. Jesus Dorantes L., Escuela de Biologics, Universidad Veracru- zana, Jalopa; Arturo Goma-Pompa, Instituto de Investigaciones Sobre Recursos Bioticos; Pilar Fernandez and Jose Sarukhan, Universidad National Autonoma De Mexico for help with the field experimenis in Mexico which were carried oui in conjunction with the course Biolog); 247, Harvard University with Iinancial support from the Atkins fund.
We would also like to thank Drs. R. and A. Tryon from the Gray Herbarium, Harvard' U., C.L. Remington, Yale U., J.G. Franclemont, Cornell U., T. Swain, Boston U. for helpful discussions.
Many people have helped in the compilation of the arthropod fern list. Most of their names are listed in Appendix 1 as personal communications (p.c.) or in litt. as well as D. Johnson, Ohio State and J. Slater, U. Conn.
Biochemical and Evolutionary Aspects of Arthropod Predation on Ferns
Psocidae : Psocus distinguendus Sadleria Perkins ( P )
Hawaii Zimmerman, 1948
COLEOPTERA Alticidae ( = Chrysomelidae) : Apthom sp. P. aquilinum Manobia sp. 1 P. aquilinum M. sp. 2 P. aquilinum
Anthribidae: Homocloeus n. sp. 1 tree ferns Homocloeus n. sp. 2 tree ferns
Ormiscus floridanus (Leng) ferns Phaenorheriopsb n. sp. tree ferns Trigonorhinus ronmdatw ferns Leconte
Carabidae: Several native Hawaiian tree ferns SPP. ( 4 (assoc.)
Cerambycidae : ?Cornallb sp. P. aquilinum Sybra sp. P. aquilinum Tmesisfernus sp. 1 P. aquilinwn T. sp. 2 P. aquilinum Unidentified sp. 1-sp. 5 P. aquilinum
Cryptophagidae: Unidentified sp. (s) Cysfopteris fragilis
M. montemgus (Zimm.) fern Tahiti Is. Zimmerman, 1957 M. nitidus (Zimm.) (0) Asplenium nidus Rapa Is. Zimmerman, 1957 M. obesus (Zimm.) (0) ferns Rapa Is. Zimmerman, 1957 M. orofenae (Zimm.) Cyathea sp. Tahiti Is. Zimmerman, 1957 M. paenulatus (Zimm.) (0) Aspleniwn nidus; Cyathea Rapa Is. Zimmerman, 1957
D. nigella Hardy (assoc.) ferns D. notha Bock (g) P. aquilinum
D. sadleria Bryan (m) Sadleria cyafheoides
Pipunculidae (assoc.-parasite): Pipwculus alienus (Hardy) ?leafhoppers over
Cibotiwn and Nephrolepis P. amplus a aid^ over Nephrolepis sp. P. cornutus (Hardy) over Nephrolepis sp. P.filicicolus Hardy over Nephrolepis exaltata P. jumtor Perkins ?leafhoppers over Nephro-
lepis and ferns P. megameris Hardy over Cibofium
P. obscuratus Hardy over Cibotium chamissai K. (assoc. with Neso- phrosyne sp. and Neso- sydne ipomoeicola Kirk)
P. timerlakei Hardy over Cibotium chamissai (assoc. with Nesophrosyne and Nesosdyne ipomoeicola)
M. (= Sthemrusoides) P. oquilinrun punctipemis Linnavuori Orthotyhu kassandra Sadleria (Kirk.) (PI Pseudoclerah moroi creeping fern Kirk. (assoc.) Stenodema hokatm P. aquilinum (Fab.1 (PI Tenthecoris bicolor ornamental ferns k o t t (PI Nabidae : (assoc.) Nabb blockburni (White (PI N. curtipemis Blackburn N. Iusciosw White (P)
N. pele (Kirk.) (0) N. siloestris (Kirk.) (0)
Pentatomidae: (assoc.) Aelia acuminalo L. (P)
Jalla dwnosa L. Zicrono caeruleo L.
ferns Hawaii Zimmerman, 1948
Hawaii Hawaii Hawaii Hawaii
Z i e r m a n , 1948 Zimmerman, 1948 Zimmennan, 1948 Zimmerman, 1948
Areopodidae (= Delphacidae) : Criomorphus pferidis P. aquilinum Brit. Is. (Spinola) Nesodyne (= Ilburnia) Sadleria cya fkoides; Hawaii ipomoeicola (Kirklady) (P) Cibotriun sp. N. amamau Muir Sadleria cyatheoides Hawaii N. nephrolepidis (Kirk.) Nephrolepis exaltata Hawaii Nofhorestias badia Muir ferns Hawaii N. swezeyi Muir Aspidium fern Hawaii Nesoresfias filicicola Ehphoglossum gorgoneum; Hawaii Kirk. Ciborium; ferns
Kimball, 1965; D. Schweitzer (p.c.) Wieczorek, 1973
Swezey, 1922
Zimmerman, 1948
Lawton, 1976
Haliophyk (= Erio- many ferns Hawaii pygodes) euclidias (Meyrick) H. spp. several ferns; Acrostichum; Hawaii
Aspidium cyatheoides Loconobirr (= Mameslra) P. aquilinum Brit. Is. contiqua (Den. und Schlif.) (P) (assoc.) L. oleracea (L.) (P) P. aquilinum Brit. Is. Lawton. 1976 (assoc.) Orthodes crenuhta Onoclea sensibilis L. Penn. Schweitzer (p.c.) (Butler) (P) Papipema inquoesita Onoclea semibilis L. Can.-111.-Wash.. Forbes, 1954 Gr. and Robins. (r) D.C. P. n. sp. near pterisii (r) Pteretis pennsylvanica N.E. USA D. Schweitzer (p.c.)
(Willd.) P. pterisii Bird (I) P. aquilinum E. Can.-N.Y.- Forbes, 1954
Pa. P. speciosissima Gr. and Osmunda regalis L.; 0. E. Can.-N.Y.- Forbes, 1954 Rob. cinnamomea Ga.
Biochemical and Evolutionary Aspects of Arthropod Predation on Ferns
Appendix 1 (continued)
Arthropod taxon Fern host Locality Reference
P. stenocelis (Dyar) (r) Woodwardia virginica N.E. USA Forbes, 1954 (L.) Sm.
Peridroma margaritosa P. aquilinum (Haworth) (= P. saucia Huebner) (P) Phlogophora meticulosa P. aquilinum (L-) (PI Polia adjuncta (his- P. aquilinum duval) (P) .
Yponomeutidae (= Walshiidae) : Bafrachedra sophroniella Aspidium cyafheoides Hawaii Walsingham(s) B. Iomenfella Wals. fern Hawaii B. bedeliella Wals. (s) Asplenium nidus;Elapho- Hawaii
glossurn reticukmm; Dryo- pteris parasilica
B. sp. (m) Pteris irregulnris Hawaii B. SPP. (4) (?m) Polypodium spectrum Hawaii
(?part) Euhyposmocoma ekaha Asplenium nidus Hawaii (Swezey) E. trivitella Swezey (m) Elaphoglossum reticulafum Hawaii Hyposmocoma spp. ferns (several)
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