Insect Predation of Seeds and Plant Populations Dynamics

8/8/2019 Insect Predation of Seeds and Plant Populations Dynamics

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MAINE AGRICULTURAL AND FOREST EXPERIMENT STATION

University of Maine

February 1997February 1997February 1997February 1997February 1997Technical Bulletin 163Technical Bulletin 163Technical Bulletin 163Technical Bulletin 163Technical Bulletin 163

Insect Predation of Seeds and Plant

Population Dynamics

Jianxin Zhang

Francis A. Drummond

Matt Liebman

and

Alden Hartke

ISSN 10701524


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Insect Predation of Seeds and

Plant Population Dynamics

Jianxin ZhangResearch Associate

Francis A. Drummond Associate Professor

Matt Liebman Associate Professor

and

Alden HartkeGraduate Student

Department of Applied Ecology and Environmental SciencesUniversity of MaineOrono, Maine 04469-5722


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ACKNOWLEDGMENTS

The aut hors wish t o th an k Dr. Elean or Groden a nd Dr. Eric

Gallandt for critically reviewing t he m an uscript a nd Dr. Richa rdStorch for editorial a ssistan ce. This work was fun ded by th e Un ited

States Department of Agriculture from a special CSRS research

grant for potato ecosystems.


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ContentsContentsContentsContentsContents

In t rodu ction ...................................................................5

Predisper sa l Seed Preda t ion ......................................... 5

Postdisper sa l Seed Preda t ion ......................................10

Seed Pr edat ion And P lant Populat ion Dyna mics .......15

Plan t Popu lat ion Recru itm ent ............................... 15

Seed Disper sa l ........................................................17

Spa t ial Pa t terns of Plan ts ......................................17Adapt a t ion ..............................................................18

Plan t Community Dyna mics ..................................21

Weed Control With Seed Preda tors .............................22

References ....................................................................25


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MAFES Technical Bulletin 1636

Table 1. A list of insect seed predator species.

Order Family Species References

Coleoptera Bruchidae Acanthoscelides fraterculus* Green and Palmbald1975

Bruchus atromarius* Crawley 1992Mimosesta mimosae* Traveset 1990Mimosesta nubigens* Traveset 1990Sennius abbreviatus* Crawley 1992Stator vachelliae Traveset 1990

Carabidae Amarasp. Imms 1948Amarasp. Zhang 1993Evarthus alternans Best and Beegle 1977

Evarthus sodalis sodalis Best and Beegle 1977Harpalus fuliginosus Kjellsson 1985Harpalus penslylanicus* Best and Beegle 1977;

Manley 1992Harpalus rufipes Zhang 1994Omophronsp. Imms 1948Pterostichus chalcites Best and Beegle 1977Pterositichus lucublandus Best and Beegle 1977Zabrussp. Imms 1948

Curculionidae Curculio glandium* Crawley 1992Diethusasp.* Auld 1986Erytenna consputa* Neser and Kluge 1985Melanteriussp.* Auld 1983Melanterius acaciae* Auld and OConnell

1989Pseudanthonomus hamamelidis*DeSteven 1983Pseudanthonomus virginiana* Crawley 1992Rhinocyllus conicus Kok and Surles 1975Rhyssomatuslineaticollis Franson and Willson

1983

Diptera Anthomyiidae Hylemya sp.* Hainsworth et al. 1984;Crawley 1992

Pegohylemyia seneciella* Crawley 1992Scatophagidae Gimnomera dorsata* Molau et al. 1989Tephritidae Aethes deutschiana* Molau et al. 1989

Euaresta aequalis* Hare 1980Neospilota signifera* Louda 1982Orellia occidentalis* Lamp and McCarty

1982Orellia ruficauda* Crawley 1992Paracantha culta* Lamp and McCarty

1982Trupanea wheeleri* Louda 1982

Urophora formosa* Louda 1982Urophorasp.* Crawley 1992

Hemiptera Miridae Lygus boralis* Crawley 1992


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MAFES Technical Bulletin 163 7

Table 1. continued.

Order Family Species References

Hymenoptera Eurytomidae Eurytoma sp.* Auld 1986Formicidae Paratrechina vividula Alvarez-Buylla and

Martinez-Ramos 1990Messor arenarius Abrahamson and Kraft

1965Solenopsis geminata Risch and Carroll 1986

Lepidoptera Arctiidae Tyria jacobaeae* Crawley and Gillman1989

Carposinidae Carposina autologa Neser and Kluge 1985

Cochylidae unidentified sp.* Louda 1982Coleophoridae Coleophora alticolella* Randall 1986Gelechiidae Sophroniasp.* Louda 1982Geometridae Eupithecia cimicifugata* Willson 1983Heliodinidae Heliodines nyctaginella* Kinsman et al. 1984Incurvariidae Tegeticulasp.* Keeley et al. 1984Noctuidae Dioryctyra sp.* Merkel 1967

Barbarasp.* Koerber 1962Hadenasp.* Pettersson 1991

Oecophoridae Depressaria pastinacella* Sheppard 1987Olethreutidae Laspeyresiasp.* DeSteven 1983; Kraft

1968; McLemore 1975;Werner 1964

Pieridae Anthocharis cardamines* Duggan 1985Pterophoridae unidentified sp. Louda 1982Pyralidae Homeosoma electellum* Carlson 1967

Homeosoma stypticellum* Lamp and McCarty1982

Tortricidae Clepsis peritana* Louda 1982Phaneta imbridana Hare 1980Epiblema scutulana* Leeuwen 1983Cydia fagiglandana* Nielsen 1977; Nilsson

and Wastljung 1987

Phaneta imbridiana* Hare 1980

Orthoptera Gryllidae Hygronemobiusp. Alvarez-Buylla andMartinez-Ramos 1990

Thysanoptera Philoeothripidae Haplothripssp.* Louda 1982Thripidae Frankliniella minuta* Louda 1982

Frankliniella occidentialis* Louda 1982

* predispersal insect seed predator


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Pr edispersal seed pr edation ofCirsium a rvense, Can ada th istle,

by Orellia ru ficaud a(Dipt era : Teph r itidae) occurs in 20% to 85% of

th e seed hea ds, and t he pr oport ion of dam aged seeds per a tt acked

head a vera ges 20%80%, depending on geogra ph ical locat ion a nd

sam pling da te (Forsyth e an d Wat son 1985). Although t he impa ct of

th is seed preda tor is not severe enough t o resu lt in elimina tion of

th is plan t from a n a rea where it is comm on, it is suspected t o be an

import an t factor in t he population regulation ofC. arvense(Forsythe

an d Wat son 1985).

Quite often a complex of predispersal seed predators attack

plants . Kjel lsson (1985) found two species of mice in the

myrmecochorous Carex piluli fera(Cypera ceae) (plan ts , dispersed

by an ts ) fields before seed fall. Dur ing t he n ight , th e mice climb th e

Carextu fts, somet imes rising an d r eachin g out for fru iting spikes.

Norma lly, th e culm is bitt en just below th e spikes, resu lting in an

oblique cut similar to cuts seen on damaged culms in the field.

These m ice cons um e diaspores from 20 to 25 culm s over t wo hour s.

In addition to seed reduction from the mice, the ant species

S olenopsis flavicollis is a major harvester ofC. pilulifera seeds

(Kjellsson 1985). It is estimated that S. flavicolliscan reduce th e

seed pool by 21.3%.

A northern Swedish population of Bartsia alpina, an arctic

per enn ial h erb, is foun d t o suffer h igh levels (norma lly 40%50% of

th e fru its) of predispersa l seed redu ction from t he combined p reda -

tion by larvae of two insect species: Aethes deutschinana(Lepi-

d o p t e r a : T o r t r i c i d a e ) a n d G i m n o m e r a d o r s a t a ( D i p t e r a :

Scatophagidae), both common seed predators of rhinanthoid

Scrophula ria ceae pla nt s (Molau et a l. 1989). The level of tort ricid

at ta ck is more or less const an t between years, an dB. alpin aseems

to be th e primar y host plan t for A. d eutschiana. The scatophagid

at ta ck is lower th an th e tort ricid att ack, but more var iable between

years. This is probably due to th e fact th at th is preda tor ha s an oth er

plant species, Pedicularis lapponica, as its main host. Also, the

degree of its attack on B. alpinadepends on the ability of P.

lapponica to escape in time by shedding its seeds before adult

emer gence of t his s cat oph agid (Molau et al. 1989).

The int ensity of predispersal seed pr edat ion by insects varies

with plant individuals. Tra veset (1990) investigated two bru chid

beetles pr eying on seed ofAcacia farnesian a. She foun d th at th e

inten sity of seed predat ion varies notably among shr ubs, with out

showing an y seasona l pat ter n. Assum ing th at a dult bru chids move

among shr ubs an d tha t th ey can live up to thr ee mont hs an d have


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several generations within the five- to six-month fruiting season,

an increase in seed pr edat ion m ight be expected du ring t his period.

Predispersal seed predation by insects can be a key factor

determining the distribution of plant populations. Louda (1982)

invest igated the variat ion in temperate shrubs Haplopappus

squarrosus and H. venetusover an elevational gradient in the

coastal sage scrub vegetation of San Diego County, California.

Haplopappus squarrosusand H. venetusare characteristic of

Californ ia coast al sh ru bs, th e densities being h igher on th e coast

th an inlan d (Loud a 1982; Louda et al. 1989). In San Diego Coun ty,

th ey replace each oth er a long an 80 to 100 km gra dient from t he

coast t o inland m oun ta ins;H. squarrosusis foun d inlan d, whereas,

H . venetu spredominat es in coast al a rea s. Experiment al exclusion

of seed predat ors a t sites along a gradient from t he coast to inland

mountains demonstrates two phenomena related to seed preda-

tion. First , predispersa l seed pr edat ion limits seed inpu t t o th e soil

and subsequently affects local seedling recruitment for both spe-

cies. Second , th e net effect of th ese losses on ad ult plan t d istr ibu-

tion along the gradient changes as the physical conditions and

impact of other predators varies. For the inland species, H.

squarrosus, predispersal seed predation is the most important

factor explain ing both local recru itm ent an d repr odu ctive age class

plant distribut ion over t he grad ient . Seedling recru itmen t is pro-

portional to the number of uneaten seeds; predation lowers seed

release different ially an d is m ost severe a t th e coast . For cont rol

plant s (with seed pr edat ors, without pesticides), th e distribut ions

of both seedlings an d pr ereproductive age class plan ts exhibited t he

same trend as the observed reproductive plant distribution. But,

for plants with seed predators excluded (with pesticides), the

distribut ions of both seedlings an d pr ereproductive age class plan ts

corr esponded to th e repr oductive age class plan t distribut ion along

the gradient. Louda (1978) concluded that with H. squarrosus,

predispersal predators limit local recruitment and confine plant

abundance to the inland portion of its potential niche. For the

coastalH. venetus, seed pr edat ors also restr ict seedling esta blish-

men t. In addition, seedling morta lity, cau sed prima rily by herbi-

vores and not by seed predators, is disproportionately severe

inlan d. Together, h igher seed losses an d h igher seedling morta lity

in th e inlan d ar ea restr icted th e observed distribut ion ofH. venetu s

to th e coas ta l port ion of its poten tia l ra nge (Loud a 1978).


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an ts can not find seeds u nder t he soil su rface. A second differen ce

relat es to the t iming of preda tion beha vior: rodent s ar e noctu rn al,

while ants are mostly diurnal. Large seeds are utilized first by

rodents, a shift to small seeds occurs only after most of the large

seeds have been utilized. Rodents are primarily seed predators,

while ants act also as seed dispersers. The interference of ant

preda tion from r odent p reda tion is minimal as an ts cont inue th eir

fora ging even wh ile seeds in t ra ys ar e repla ced (Abra msk y 1983).

Compet ition ma y occur between an ts an d r odent s for seeds in low

densityAcaciast an ds (Holmes 1990).

Ant s sh ow an inter esting seed preferen ce behavior. Risch an d

Carroll (1986) found that in feeding preference field studies, the

am oun t of each seed t ype removed by an ts was st rongly influen ced

by the am oun t a nd k inds of oth er seeds in t he immediat e area. A

st rongly preferr ed seed is removed less frequ ent ly if it occur s in t he

midst of non-preferr ed seeds. Non-preferr ed seeds ar e ta ken mu ch

more r eadily if t hey occur with pr eferr ed seeds (Risch a nd Ca rr oll

1986). Studies allowing ants free passage to seeds, but excluding

larger seed predators show that seed predation of the tropical

pioneer tr ee, Cecropia obtusifolia, was not significantly different

from uncovered control seeds, indicating that ants were the pri-

mary seed predators. The distribution of seed predation rate by

an ts after four days of experimen ta tion was bimodal, suggesting

once an ts discover a dish of seeds, all of th em a re t ak en (Alvarez-

Buylla an d Ma rt inez-Ramos 1990).

Seed predat ion by the Cara bidae was report ed as early as th e

1880s (Forbes 1880, 1883; Johnson and Cameron 1969; Webster

1880, 1900). Nitzsche (1893) reported that carabid beetles of the

genus Harpalusdest royed up t o 80% of th e seed an d seedlings in

nu rsery beds. Predat ion ra te by car abids var ies with pr edator an d

prey species. Lund and Turpin (1977) tested predation by five

Carabidae species on six seed species. In a test to determine if

beetles would attack weed seeds in the laboratory, Harpalus

pensylvanicus damaged more seeds than other carabid species.

However, the number of seeds damaged varied with the seed

species. Pterostichus chalcitesand P. lucubland usdamaged simi-

lar numbers and species of seeds, but only chickweed, Stellaria

media, was damaged in high numbers. The carabid Evarthrus

soda lis soda lisda ma ged only a few seeds of an y species (Lun d a nd

Tur pin 1977).

Fu rt her st udy of predation byHarpalu s pensylvanicusshowed

that predation rate varies with seed species. On the basis of

pr edat ion pr eferen ce over a 40- hour period, seed species could be


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grouped int o t hr ee to five cat egories (Lun d an d Tur pin 1977). Best

and Beegle (1977) found that H. pensylvanicusand Evarthrus

alternatesfeed on m an y kinds of seeds with pr eferen ce for smooth

dock seeds, barnyard grass seeds, and yellow foxtail seeds. Lund

and Turpin (1977) found that H. pensylvanicusprefers green

foxtail, Setaria viridisvar. major, over other seed species tested.

The size of seeds tested might influence the number of seeds

da ma ged in one of two ways. Lar ger seeds pr ovide more food per

seed, an d it r equires fewer seeds to satiat e th e an imal. Also, th e size

an d sh ape of th e seed might affect t he ease with which t he beetle

can ha nd le and open t he seed. Pr eferen ce for one seed species over

an oth er m ight well be due to the ea se of ha ndling an d opening of th e

seed rather than selection based on textural or chemical clues

(Lun d an d Tur pin 1977).

Although H. pensylvanicusis usually a postdispersal seed

preda tor (Best a nd Beegle 1977; Lun d a nd Tur pin 1977), it ma y also

act as a predispersal seed predator in specific habitats. Manley

(1992) found that H. pensylvan icus adults have more impact on

seed production prior to seed maturity than afterwards. Beetle

populations in 1992 were highest prior to seed maturity. Caged

adu lts fed on both individua l mat ur e seeds of grasses a nd develop-

ing seed heads. Adults readily fed on inflorescences of crabgrass

an d fall pan icum (whose heads a re n ear or on th e soil surface), but

not on green foxtail (whose seed heads are distant from the soil

su rface), th ough beetles fed on ind ividual gr een foxta il seeds. Th is

suggests tha tH. pensylvan icus may r eadily at ta ck imma tu re seeds

or seed head s when t hey ar e near th e soil sur face.

Considera ble resear ch ha s been condu cted on t he postdispersal

seed predation of the European carabid Harpalus rufipes. This

species is primarily a seed predator (Briggs 1965; Curtis 1860;

Forbes 1880, 1883; J ohn son an d Cam eron 1969; Luff 1980; Sku hr avy

1959; Webster 1880, 1900; Zha ng 1993; Zha ng et al. 1994; Zna men skii

1926); however, when seeds are in low relative abundance, H .

rufipes will feed on small insects (Chiverton 1987; Coaker and

Wiliams 1963; Cornic 1973; Dempster 1967; Hamon et al. 1990;

Rivar d 1966; Sun derlan d 1975; Sun derlan d et a l. 1987; Zha ng et a l.

1994). Adults have been observed to feed on the seeds of 29 of 38

species of plants in the laboratory (Briggs 1965; Zhang 1993).

Pr eferen ce for seed species is sh own by H. rufipesadu lts (Zha ng

1993). Gra sses ar e a pr eferr ed type of seed along with sma ll seeds

such as comm on lambsqu ar ter s, Chenopodium album, an d dande-

lion, Taraxacum officinale. Seeds of species in t he Cr ucifera e ar e

the least preferred. The mode of feeding is associated with seed


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species as is t he fun ctiona l response (Zha ng 1993). Adu lts exh ibit

a t ype II fun ct iona l response (Pr ice 1984) to preferred seeds a nd a

type I r esponse to less preferr ed seeds.

Lar vae ofH . rufipesar e also seed pr edators. Lar vae scra pe soil

away from th e term inal cell of th e tu nn el with th eir m an dibles and

press it in to th e side of th e bur row with th e dorsa l sur face of th e

hea d. Seeds a re carr ied in th e ma ndibles before being embedded in

th e side of th e bur row with t he h ead. Ther e is often a closely pa cked

cache of seeds just above the terminal cell where the larvae

consu me single seeds (Thiele 1977). Luff (1980) found that second

instar larvae ofH . rufipesfed on 18 out of 24 species of seeds offer ed

in a choice test . Eight favora ble species were eat en by a t least six

of ten lar vae t o which th ey were offered. Th ese species wereLolium

perenne, Festuca rubra, Chenopodium album, Agrostis tenuis,

Dactylis glom erata , Trifolium repens, S enecio jacobaea, and

Medicago lupulina. The remaining unfavorable species were

Brassica rapa, Cardam ine am ara, Scabiosa columbaria,Brassica

oleracea, Hypericum perforatum, Antennaria dioica, Campanula

rotundifolia,Heracleum sphond ylium, S isymbrium officinale,Bras-

sica napus, Fil ipendula u lmaria , Geum urbanun , Hesperis

matronalis, S cutellaria galericu lata, and Solanum dulcamara.

When given a choice among six favorable seeds offered two at a

time, th e ran king was similar to tha t when th e same seeds were

offered with out choice, alth ough a m ore dist inct division a ppea red

between grasses an d C. album, which were highly preferred, a nd

th e rem aining t wo lesser pr eferred seed species.

Germina ting seeds ar e also dam aged byH . rufipes. Lar vae feed

on the endosperm of germinating seeds of perennial rye grass

(Loliu perenn e). The larval growth ra te is more ra pid with germ i-

nating seeds of lambsquarters, C. album, groundsel, Senecio vul-

garis, and th e gra sses Agrostis tenu is, Festuca ovin a, and Phleum

pratense, tha n with th ose of perenn ial rye grass a nd cereals. There

are no differences between the feeding rate on germinating and

non-germina ting seeds ofL . perenn e. The m ean nu mbers of germi-

na ting an d non-germina ting seeds eat en by ten larva e were 2.8

0.4 and 2.8 0.3, r espectively (Luff 1980).

H. rufipesis associated with cultivated habitats and is most

abu nda nt in sm all fields as compa red t o large agricultu ra l fields

(Tra veset 1991). Another cha ra cter istic of fields t ha t ma y affectH .

rufipesabu nda nce is weediness. Speight an d Lawt on (1976) used

an ar tificial pr ey to test th e effect of th e weed Poa ann uain cerea l

fields on the abundance of carabids, including H. ru fipes. With in

one field, areas of high weed cover had more predatory ground


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beetles, and a rt ificial pr ey suffered sign ifican tly grea ter mort ality

than areas with few weeds. Diversity of weed species has been

suggest ed to be import an t for groun d beetle popu lat ions (Mur doch

et a l. 1972; Pimen ta l 1961; Speight an d La wton 1976). The r elat ion-

ship between beetle activity and th e frequen cy an d abu nda nce of

Poaannuais probably complex, but it is likely tha t th e role th at th e

weeds play in protecting t he p redat ors from weat her extr emes, i.e.,

insolation du ring th e day, an d desiccat ion, both dur ing the da y and

at night , is import an t (Speight an d Lawt on 1976). Rivard (1966)

foun d h igher cat ches of car abids in a reas of higher hu midity, and

Thiele (1964) cons iders t ha t r elative hu midity is a key factor in th e

abundance of the majority of carabids and that microclimate in

vegeta tion is very importa nt . High weed densities provide a h igh

rela tive hu midity. It is also possible th at th ere is an indir ect effect

of weed density du e to the a bun dan ce of na tu ra l prey, which ma y

be more comm on in dense weed pat ches (Speight an d Lawt on 1976).

However, exception to th e weediness h ypoth esis exists. Pu rvis an d

Cur ry (1984) foun d th at none of th e domina nt car abids th ey studied

respond positively to weediness. Although, the activity of P.

melanariusappea red t o persist longer in weedy plots in Septem ber,

both this species and H. rufipeswere equally active in all plots

dur ing their peak a bun dan ce in August. One possible reason m ay

be th e crop (beet) provides sha de an d h igh relat ive hu midity even

in t he absen ce of weeds.

Cultivation may favor H. rufipesbecause of larval require-

ments for seeds as food. An open soil surface encourages weed

growth , an d H . rufipeslar vae would be sh ort of food in a field k ept

completely weed free (Luff 1980). After using pitfall traps to

investigate the carabid fauna of arable land, Scherney (1960)

concluded t ha t cert ain Car abidae (H . rufipesincluded) were as so-

ciated with cultivation; the numbers taken in pitfall traps in

differen t h abit at s were in t he following order: wheat fields > bar ely

> potato > clover > grass meadow > densely weed-covered waste

ground. Although agricultural monocultures are considered un-

stable habitats, they may provide stable conditions for species

dependent on relatively bare, loose cultivated soil, such as H .

rufipes(Luff 1980).

Other environmental factors also have an impact on seed

predation rate by carabids. Brust and House (1987) investigated

w e e d s e e d l o s s i n c onve n t iona l t i l l a nd no - t i l l s oybe a n

agroecosystems. Seeds of four broadleaf weed species (ragweed,

pigweed, sicklepod, and jimson weed) an d one gr ain crop species

(whea t ) were pr ovided in a free choice design with densities of 10,


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25, and 50 seeds per 24 cm 3 of soil. Approximately 2.3 times more

seeds overall, and 1.4 times more large seeds as a group were

consu med in no tillage systems t ha n in convent iona l tillage systems.

In low-input, no-tillage treatments, large ground beetles (15

25 mm ) an d m ice preferent ially fed on t he la rge seed species, while

sma ll car abids (< 15 mm), ant s a nd crickets, fed alm ost exclusively

on the smaller seed species. Carabid beetles were responsible for

more th an ha lf of all seeds consu med (Brust an d H ouse 1987). The

difference in predation rates between no-tillage and conventional

tillage systems can be explained by the differences of the seed

predator abundance as a result of soil disturbance. In the south-

eastern United States, conventional tillage systems (moldboard

plow/disk) gener ally support fewer soil ar th ropods t ha n n o-tillage

system s (Blum bur g an d Crossley 1983; House a nd All 1981; House

an d P ar melee 1985). Soil distu rba nces in n at ur al ecosystems can

also depress soil arthropod numbers, resulting in a concomitant

reduction in seed predation (Mittelbach and Gross 1984).

SEED PREDATION AND PLANT POPULATION

DYNAMICS

Plant Population RecruitmentPlant Population RecruitmentPlant Population RecruitmentPlant Population RecruitmentPlant Population Recruitment

Seed predation m ay influence plant s at both t he populat ion a nd

individua l levels. At th e populat ion level, poten tia l effects includ e

(a) lower r ecru itm ent ra te due t o reduction in occupan cy of sa fe

sites (Louda 1978) su ita ble for germ ina tion an d esta blish men t, (b)

discontinuous recruitment due to periodic or mast fruiting and

th e accompa nying sat iation of seed preda tors (J an zen 1971a), an d

(c) alterna tion of adult distribut ion, du e to density dependent seed

predation (Janzen 1971a). The potential consequences of seedpredation at the individual level have been less widely explored.

Seed production an d spa tia l locat ion m ay influence th e severit y of

pr edispersa l preda tion on differen t in dividu als (Moore 1978). The

ecological resu lt is th at t he r elative cont ribu t ion of some adu lts t o

successful seed production will be great er t ha n th at of oth ers, an d

ma y be so consisten tly, from year t o year. If these t ra its a re h eritable,

th e evolut ionar y result is a selective force upon a dult cha ra cter istics

th at confers r elative escape from pr edat ion (DeSteven 1983).

Evalua tion of preda tion in seed bank dynam ics is eith er t rivialor surprisingly difficult. Seed consumption is a major gustatory

str at egy th at cau ses significan t seed losses. So in t he t rivial sense,

seed preda tion, like an y mort ality factor cau sing a consisten t loss

of young, will influence popula t ion ecology an d evolu t ion . Consis-


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ten t losses have a poten tial impact on plant a bun dan ce, distribu-

tion, competitive status, life cycle traits, and other adaptations.

Differen ces in da ma ge among ind ividu als or between species can be

significan t even where t he m agnitu de of the loss is sma ll.

Seed predat ion ra te m ay be relat ed to seed size. Reader (1993)

found adding a cage to reduce seed predation, especially by ants,

did n ot increase s eedling emergen ce significan tly for sm all seeds

(0.060.14 mg). In cont ra st , seedling emer gence increa sed signifi-

can tly for lar ger seeds (0.1512.2 mg) (Reader 1993). Seed pr eda-

tion not only affects t he n um ber of seeds, but also reduces th e seed

viability. Andersen (1988) compared two methods of studying

insect preda tion on seeds in Aust ra lia. The convent iona l meth od

(inspecting insect attack symptoms) indicated that insects at-

tacked only 2%, 10%, 28%, and 1% respectively ofEucalyptus

baxteri, Leptospermum myrsinoides, L. juniperinum, and Casua-

rina pusilla seeds, whereas bagging experiments indicated that

insects reduced seed production by 66%, 64%, 44%, and 83%,

respectively. Therefore, if th e bagging experimen ts reflect a more

accur at e pictu re of preda tion, th en insect seed pr edat ors m ay cau se

far great er losses th an th ey appear to (Ander sen 1988).

How important is seed predation to recruitment in stable

populat ions of long-lived per enn ials? The im porta nce of seed losses

to population recruitment at any point in time is related to the

abundance of safe sites. Insect seed predation rate can be very

high, up to 100% of the seed population (Sallaban ks a nd Cour tn ey

1992). However, t hese losses do not n ecessar ily ha ve an im porta n t

impact on populat ion recru itmen t becau se (a) in most years pr eda-

tion is not 100%, (b) in m ost year s r ecru itmen t appea rs to be limited

by a r ar ity of sa fe sites a nd not by seed su pply, an d (c) t he losses do

not pr event th e establishment of large seed ban ks (ran ging from 30

to 1,100 viable seeds per m 2) potentially capable of exploiting

temporary conditions favorable for recruitment (Sallabanks and

Courtney 1992).

Seed-feeding insects, as comp ar ed with leaf-feeding ones, often

destroy a large fraction of their food supply (Janzen 1971a).

Although seed predat ion r at e may be high on t he a verage, it is also

highly variable (House and Parmelee 1981). The dynamics of a

seed-predator system seems to depend primarily on how seed

preda tor populations tr ack th eir variable resour ces in t ime an d

space (Solbreck and Sillen-Tullberg 1986). At present, few seed

preda tion models ar e available. Reduction of the seed ban k t hr ough

seed predation can be expressed as an exponential decay curve

(Boucher 1981):


17/32


18/32


pioneer t ree seeds and a ra pid tu rn over r at e of its seed bank (1.02

to 1.07 years ) (Alvarez-Buylla a nd Mar t inez-Ram os 1990).

Whelan et al. (1990) examined the spatial and temporal pat-

ter ns of postdispersa l seed preda tion of vert ebrat e-dispersed plan t

species (Cornus drum m ondiiand Prunu s am ericana) in temperat e

woodlan d a nd old-field h abit at s. Rat es of seed loss by all predat ors

including insects va ried with microhabita t (near logs, tr ee tru nk s,

an d open forest floor), ma croha bita t (old-field, forest ), plan t spe-

cies, year , an d t ime of disper sal with in a year . The levels of fina l

mort ality of seeds did not vary with microhabitat or t ime of dispersal,

but did var y between ma crohabita ts, plant species, and years.

As discussed previously, a study conducted by Louda (1978)

showed tha t t he plan t H . squarrosusis confined t o inla nd port ions

of its potent ial niche du e to th e seed predat ion of insects. In tu rn ,

th e distr ibut ion of seed resour ces ma y affect s eed preda tion. Seed

preda tion in relat ion to pat ter ns of pod (and seed) distribut ion wa s

examined in five samples of the common milkweed (Asclepias

syriaca), in t est s of the resour ce-concent ra t ion effect both wit h in

an d between plan ts (Fra nson an d Willson 1983). Plant s with large

clusters of pods produced more undamaged pods, and, by this

measu re, were more successful th an plant s with sma ll cluster s.

AdaptationAdaptationAdaptationAdaptationAdaptation

Theoretically, seed predation, like other forms of predation,

sh ou ld cau se two types of response by th e exploited pla nt popula-

tion. The first is adap t at ion, via s election for morph ological, chemi-

cal, temporal, an d spa tial m echa nisms of predat or avoidance. The

second is modification of numerical and spatial occurrence, via

elimina tion a nd r edistribut ion of better -ada pted individua ls in t he

population through differential patterns of attack (Harper 1969;

Janzen 1969, 1971a, 1971b; Louda 1978). Although variability in

th e dam age to seeds is genera lly high, seed predat ion is t hought to

represent a strong selective force acting on protective structures

(Janzen 1969, 1970; Smith 1975); dispersal phenology (Heithaus

1981; J an zen 1971b; Silvert own 1980); an d dispersa l meth od (Beat tie

an d Lyons 1975; ODowd a nd Ha y 1980). The d ispersa l of seeds

from the parent plant and its surroundings is often thought to

decrease the risk of predation and pathogen attack (Augspurger

1983; Ha rper 1977; J an zen 1969; Wilson an d J an zen 1972). Hence,

it h as been su ggest ed for severa l genera (e.g., Viola, Sanguinaria,

Asarum) th at seed predat ion ha s been an import an t selective force

in t he evolut ion of myr mecochory (Beat tie 1983, Beat tie a nd Lyons

1975, Heith au s 1981, ODowd a nd Ha y 1980).


19/32


Seed predation may also be a selective factor influencing the

evolution of seed protective characteristics such as spine length

an d wall thickn ess of bur rs. In a stu dy of Xanthium strumarium,

predation was found to be more intense in populations with low

mean burr length and to decline linearly with increasing burr

length (Ha re 1980). Ten popula tions ofX. strum arium occur red in

quite similar ha bitat s in proximity to each oth er, but sh owed quite

striking differences in burr size and susceptibility to seed preda-

tors. Mean burr length varied between 15.4 and 19.5 mm among

populat ions, an d th e percent age of at ta cked bur rs var ied from 3%

to 84% among populations in one year. Burr length variation

among populations is primarly genetically controlled, and differ-

ences in su sceptibility a mong populat ions persisted when plant s

were grown under uniform conditions and uniformly exposed to

insect attack. The probability of attack declined linearly with

increasing burr length under both field and experimental condi-

tions. Susceptibility was negatively correlated with mean burr

length am ong plan ts wh en plan ts from all populat ions were pooled.

Seed predat ion was a lso higher in populat ions with a lower m ean

burr length. Thus, by attacking smaller burrs, Hare (1980) sug-

gests t ha t th ese insects can be import an t na tu ral selection agents

for increased bur r size. On t he basis of oviposition behavior of the

two insects ,Eua resta aequa lis(Dipter a: Tephritidae) an d Phaneta

imbridana(Lepidopt era : Tort ricida e), th icker bur r wa lls an d longer

bur r spines could r educe the insects ability t o penet ra te bu rr s.

These cha ra cter istics were positively corr elat ed with bur r length ,

th us sh ort er bur rs m ay be more su ccessfully at ta cked becau se th ey

ar e more easily penetr at ed (Ha re 1980).

Seed predation and the coexistence of tree species in tropical

forests were studied by Hubbell (1980). Host-specific seed and

seedling preda tion can explain t he coexist ence of th e lar ge num ber

of tree species in tropical forests (Harper 1977). Janzen (1970)

noticed tha t virt ua lly all seeds un derneath th e parent are k illed by

seed predat ors, an d proposed th at only th ose viable seeds tha t a re

transported some distance from the parent have any significant

chance to escape discovery and germinate. Accordingly, such

predation should lead to a low density of, and wide spacing

between, adult trees. This would prevent any one species from

becomin g domin an t , provided t hose seed sour ces for oth er s pecies

exist to fill the available habitat (Janzen 1970). Connell (1971)

ar gued that predation was a mu ch m ore likely agent th an interspe-

cific competition to prevent single-species dominance in tropical

forest s. In optima l clima tes, predat or a bun dan ce should build un til


20/32


th ey are resour ce limited. He postu lated t ha t host-specific her bi-

vores (principally folivores) attracted by adult trees would also

discover, defoliate, and kill all seedlings in the vicinity of adult

tr ees. Seedlings ar e pr esum ably less r esista nt to defoliat ion. Again,

habit at in t he n eighborh ood of adult s of one t ree species would be

open for colon izat ion by juveniles of oth er tr ee species, an d d iver-

sity would be m aint ained. Seed density a nd th e probability of seed

survival can be expected to change with increasing distance from

th e par ent tr ee becau se fewer seeds a re expected t o be car ried to

great er dist an ces from t he pa ren t (Conn ell 1971). Regardless of th e

mode of seed dispersal, the seed shadow (seeds per unit area)

cu rve is a monotonically decrea sing fun ction of dista nce from t he

par ent tr ee (Willson 1992). On th e oth er h an d, becau se seed and

seedling predation are greater near the parent, the per capita

chance of seed survival to maturity is a monotonically increasing

function of distance from the parent. The product of the seed

shadow and the per capita chance of seed survival to maturity

cur ves describes th e density of offspring t ha t sur vive to mat ur ity at

different distan ces from t he p ar ent tr ee (Hu bbell 1980).

Tempora l patt ern s of plant repr oduction m ay also be a r esult of

seed predation. Mast seeding or mast fruiting describes the

phenomenon of synchronous production of seeds within a plant

populat ion in one year followed by an int erva l when few seeds ar e

set. This is a widespread ph enomenon a mong tempera te flora s an d

is common in hardwood trees and conifers (Harper 1977). Seed

preda tors can act a s a selective force favoring m ast fru iting, due t o

th e excessive seed losses incur red by th e asynchr onous in dividu als

th at fru it in off-peak year s. High pred ispersa l seed pr edat ion in

poor fruiting years might also enhance fruiting periodicity, if, by

preventing seeds from maturing, the resources that would have

been used for mat ur at ion ar e instead stored for u se in a su bsequent

year. The weevil Pseudanthonomus hamamelidis is host specific

an d u nivoltine on witch h azel (Ham am elis virginiana). The fluctu-

at ing patt ern of fru it production is a key featu re in u ndersta nding

th e demogra ph ic impa ct of seed pr edat ion on witch h azel (DeSteven

1983). DeSteven (1983) observed that fruit production fluctuated

between 1977 and 1980. In poor fruiting years (1977 and 1978),

oviposition sites were limited d ue t o low fru it a bun dan ce an d a tt ack

percentages on fruit crops were high. The size of the weevil

population appeared to be resource limited in such years, since

searching weevils may be unable to find particular individual

plants because they are small, have very few fruits, or are ex-

tremely isolated from conspecifics. Following poor fruiting years,


21/32


th e fru it crop in a production year sat iates th e r elat ively sma ll

weevil populat ion, with th e result t ha t seed predat ion int ensities

ar e subst an tially lower, and more seeds escape pr edat ion. Cont in-

ued high fruit production allows an annual increase in weevil

numbers and in fruit attack; however, any reduction in fruit

pr oduction following a good fru itin g year lowers weevil popu lat ion

size, and fru it a tt ack increases. The r esult for witch h azel is a pulse of

successful seed sur vival in th e occasional production year th at sa tia tes

the seed predator population (DeSteven 1983). Similar patterns of

high seed predation in years of poor seed production have been

observed in a number of forest trees, where fluctuating fruiting

pat tern s also appear to regulate seed predator populations (Abrah amson

an d Kra ft 1965; Gar dner 1977; Mat tson 1971; Miller 1973).

Ballardie and Whelan (1986) investigated the relationship

between masting and seed dispersal, and seed predation in the

cycadMacrozam ia com m un isan d foun d th at th e result was differ-

ent from DeSt evens (1983) study. They foun d t ha t d ispersa l of

seeds by opossums was poorer from source plants in a masting

population than from source plants in an adjacent, non-masting

population (Ballardie and Whelan 1986). This resulted in fewer

seeds per seeding female plant in t he m ast ing plot being dispersed

to favorable sites. Predation of seeds over the year of the experi-

ment was much more severe in the masting plot than in the

nonma sting plot. Very few seeds were t ouched by rat s in t he n on-

ma sting plot. Mast ing did not a llow an y escape from preda tion. The

absolut e num ber of seeds eat en in th e mast ing plot was m ore th an

ten t imes greater th an in th e nonm asting plot. They suggest th at

th e ma st seeding observed in M. com m un isma y not be ada ptive,

but is more likely a cons equen ce of oth er factors , which synchr on ize

flowering with in local popula tions (Ballar die an d Whelan 1986).

Plant Community DynamicsPlant Community DynamicsPlant Community DynamicsPlant Community DynamicsPlant Community Dynamics

A few stu dies have shown t ha t seed predat ion can affect plant

comm un ity stru ctu re. A na tive fire ant , S olenopsis germ inata, was

observed to harvest small seeds, especially grasses, in disturbed

habitats in wet tropical areas of Mexico and Central America

(Inouye et al. 1980; Risch an d Ca rr oll 1986). If comm on , th is an t can

lower overall abundance of many weedy species. When the ant

exhibited a st rong pr eferen ce for seeds from one plan t sp ecies, tota l

plan t bioma ss wa s significan tly lower (by up t o 50%) in plots with

ants for about the first 50 days after planting. Subsequently, the

non-preferr ed species increased, and 83 days after p lant ing, tota l

plant bioma ss was about th e same in th e presence and a bsence of


22/32


an ts. Seeds ofPaspalum distichum were highly preferr ed by th e

an ts, while Dau cus carotawere rejected. In th e absen ce of ant s, P.

distichum is competit ively super ior t oD. carota. Ant s reverse the

cour se of plan t compet ition. Th us , P. distichu m cont ribut ed little

to total weed biomass. A crop growing with ants can thus benefit

from reduced competition early in the season (Risch and Carroll

1986). Due t o seed preference, ant s m ay s elect ively rem ove domi-

na nt sma ll seeds, an d as a r esult, increase th e comm un ity diversity

and evenness (Inouye et al. 1980).

WEED CONTROL WITH SEED PREDATORS

Seed predation provides potential for classical biological con-

tr ol of weeds by seed pr edat ors (J ulien 1982). Weevils ha ve proven

to be good can didates in weed integrat ed pest ma na gemen t (IPM)

programs. Rhinocyllus conicus, a thistle-head-feeding weevil in-

troduced from France successfully controlled Carduus nutans

(mu sk t histle) at a Virginia release site (Pu laski Coun ty) six year s

after t he init ial release of 100 adu lts in 1969. Thistle density was

redu ced by 95%. In 1974 a nd 1975, about 90% of th e th istles were

at ta cked by th e weevil; more th an 10% of th e term inal h eads were

aborted. Per sistent pressu re from increa sing weevil populat ion on

th e thistles brought about dr am at ic cha nges in t he th istle problem

(Kok and Surles 1975). Furthermore, 11 years of inter-species

populat ion dynam ics st udy a t t wo release sites, Fr ederick Coun ty

an d Pu laski Coun ty in Virginia, shows th at th istle redu ction was

dra ma tic after th e explosive pha se of the weevil build-up dur ing th e

fifth year after release. Th is was followed by weevil dispersa l an d

resurgence of plant density. However, the resurgent plants were

sma ller a nd p roduced fewer bu ds t ha n th e th istles prior t o weevil

release; thus bud density during resurgence was significantly

lower t ha n th e initial density. Between 1969 and 1980, decline in

mu sk th istle bud nu mbers was 80% at th e Frederick Coun ty site

an d 97% at th e Pu laski Coun ty site (Kok a nd Pienkowski 1985).R .

conicus, when intr oduced in to San Luis Obispo Coun ty, Californ ia,

also played an important role in the control of Italian thistle,

alt hough the seed loss was only 55% (Goeden a nd Ricker 1985).

Neser a nd Kluge (1985) foun d an intr oduced seed preda tor t o

show promise in weed control in South Africa. Hakea sericea

(Proteaceae), a fire-adapted woody plant from Australia, is an

import an t weed in th e species-rich vegetat ion of the Ca pe Moun -

ta ins, Sout h Africa. This weed occur red over n ear ly ha lf a m illion

ha , mainly in moun ta inous ar eas in dense, impenetr able thickets.


23/32


The seeds r ema in viable in woody follicles th at accum ulat e on t he

plant over th e years. It was estima ted th at 75 million seeds/ha ma y

be accumulated on 15-year-old stands. From surveys of natural

enemies in Australia, two complementary seed-attacking species

were selected an d t ested for release in Sout h Africa. These a re t he

weevil Erytenna conspu ta (Coleopt era : Cur culion idae) whose lar -

vae develop in, an d cau se th e death of, youn g fru its, and th e moth

Carposina au tologa(Lepidopt era : Car posinida e) th at develops on

seeds inside ma tu re follicles accum ula ted on living plan ts. Erytenna

consputais strikingly adapt ed to its h ost a nd t o sur viving fires. The

weevil was established in South Africa after the release of small

numbers of field-collected adu lts from differen t clima t ic r egions in

Aust ra lia. Clima tic ma tching was not as import an t as h ost st ra in

ma tching in th e esta blishm ent of the weevil. Following est ablish-

ment , E. consputahas greatly (up to 86% of the total fruit

mort ality) redu ced seed accumu lat ion byH. sericeaand has s tar ted

to suppress the dense regeneration of the weed. However, addi-

tional agents may be required for an integrated control program

against th is weed from Aust ra lia (Neser a nd Kluge 1985).

Oth er insect seed predat ors t ha t m ay ha ve poten tial for classi-

cal biological control are the seed beetle S perm ophagu s sericeus

(Bruchidae) for control of field bindweed, Convovulus arvensis

(Rosenthal 1985; Rosenthal and Buckingham 1982); the flower-

and seed-feeding weevil Acallopestus maculithoraxfor control of

velvetleaf,Abutilon theophrasti(Mitt elbach a nd Gross 1984); an d

two seed predatory weevils, Ceutorhynchus turbatus and C.

parvilus, for cont rol of hoar ycress, Cardaria draba(Lipa 1974).

Inu nda tive release st ra tegies for temp ora ry (one t o five years)

reduction of weed seed banks has not become a tactic in IPM

programs. This is probably due to the expense and difficulty in

rea ring th e necessary nu mbers of seed predat ors for su ch a ma n-

agem ent t actic relat ive to th e cost of herbicides (Deloach 1978).

A promising t actic for weed ma na gemen t t ha t h as a lso not been

implemented is conservation of existing weed seed predators

(Liebman an d J an ke 1990). This tactic ha s ad vant ages over classi-

cal biological control approaches, which rely on foreign introduc-

tions. Considerations such as attack of non-target host plants or

competitive exclusion of native insect species are usually not

significant concerns (Charudattan and Deloach 1988). Carabids

an d an ts ar e ideal can didates for conser vation in n ort h t empera te

US a groecosystem s (Best a nd Beegle 1977; Blum bur g and Crossley

1983; Brust and House 1987; House and All 1981; House and

Parmelee 1985; Johnson and Cameron 1969; Lund and Turpin


24/32


1977; Man ley 1992; Mitt elbach an d Gr oss 1984; Reader 1993; Risch

an d Ca rr oll 1986; Rivar d 1966; Webster 1880; Zha ng 1993). Conser-

vation of these seed predators in agroecosystems requires that

their life systems be understood in sufficient detail so that IPM

progra ms can be designed th at minimize morta lity an d ma ximize

seed predator populat ion growth , un der th e const ra ints of ma na g-

ing insect pest s in a n a groecosystem (Bird et a l 1990). The impa ct

of factors such as tillage (Brust and House 1987; House and

Pa rm elee 1985), cover crops (Reader 1993; Zha ng 1993), rota tion

crops (Zhan g 1993), an d pest icides (Zha ng 1993) on t he p opu lat ion

dynamics of weed seed predators must be investigated for each

insect species tar geted for conserva tion. Landscape feat ur es such

as field border s, topograph y, an d spat ial patt ern an d aggregation

of far m lan ds an d forest s ha ve not been stu died in r egar ds to the

population dynamics of insect seed predators. There have been

ma ny field studies condu cted t ha t a ssess removal rat es and m ort al-

ity ra t es of seeds un der field cond itions , however, there is a gener al

dear th of inform at ion on th e qua n tificat ion of insect seed preda tor

numerical and functional responses and interference rates under

field conditions (Zhang 1993). The lack of manipulative field

studies of weed man agemen t by cons erva tion of insect seed preda -

tors pr obably reflects t he limited am oun t of resear ch t ha t h as been

conducted in the area of alternatives to herbicide based weed

man agement (Liebman a nd J an ke 1990).

We hope tha t t his review ha s provided a fra mework for u nder -

sta ndin g th e mecha nisms of insect seed pr edat ion, th e diversity of

insects that prey on seeds, and the ecological and evolutionary

consequences of insect seed predation. Insect seed predation can

play significan t r oles in r educing plan t popu lat ion gr owth , modify-

ing int ra specific an d int erspecific competit ion , shift ing spa tia l and

temporal distribution, affecting species evolution, and plant com-

munity structure, both in natural and agricultural ecosystems.

Fu rt her st udy on insect seed predat ion-plan t population dyna mics,

insect seed pr edat or beh avior, an d how to economically incorp ora te

insect seed preda tors into integra ted weed man agement pr ogram s

are all important areas of investigation with regards to insect

preda tion of seeds. We have foun d, by reviewing th e liter at ur e, tha t

there is a lack of research that attempts to link weed or plant

populat ion or comm un ity dynam ics with th e populat ion or comm u-

n ity dynam ics of insect seed pr edat ors . Most st ud ies focus solely on

either th e plan ts population dyna mics or t he in sect seed preda tors

populat ion dynam ics. The cha llenge, th erefore, in t he futu re is t o

develop a th eoret ical ba sis for t he ecology of seed pr edat ion .


25/32


REFERENCES

Abra ha mson, L.P., and K.J . Kraft. 1965. A popula tion st udy of th e

cone moth Laspeyresia toreutaGrote in Pinus banksianastands.Ecology 46:561563.

Abramsky, Z. 1983. Experiments on seed predation by rodents and

ants in the Israeli desert. Oecologia 57:328332.

Alvar ez-Buylla E.R., an d M. Mar tin ez-Ram os. 1990. Seed ban k versus

seed rain in the regeneration of a tropical pioneer tree. Oecologia

84:314325.

Andersen, A.N. 1988. Insect seed predators may cause far greater

losses tha n t hey appear t o. Okios52:337340.

Asht on, D.H. 1979. Seed har vesting by an ts in forest s ofEucalyptus

regnansF. Muell. in central Victoria. Au stralian J . Ecology4:265277.

Augspurger, C.K. 1983. Seed dispersal of the tropical tree,

Platypodiumelegans, an d t he escape of its seedlings from fungal

pathogens. J. Ecol. 71:759771.

Auld, T.D. 1983. Seed preda tion in na tive legum es of sout h-easter n

Australia. Australian J. Ecology8:367376.

. 1986. Var iation in predispersa l seed preda tion in several

Australian Acacia spp. Oikos 47:319326.

Auld, T.D., an d M.A. OConn ell. 1989. Cha nges in pr edisper sa l seed

preda tion levels after fire for t wo Aust ra lian legum es, Acaciaelongata and S phaerolobium vim ineum. Oikos54:5559.

Ballard ie, R.T., an d R.J. Whelan . 1986. Mastin g, seed dispersa l an d

seed predation in the cycad Macrozamia communis. Oecologia

70:100105.

Beattie, A.J. 1983. Distribution of ant-dispersed plants. In Dispersal

and Distribution, ed. K. Kubitzki, pp. 249267. Par ey, Ha mbu rg.

Beattie, A.J., and N. Lyons. 1975. The effect of rodent seed predation

on four species of Californ ia a nn ua l gras ses. Oecologia 33:101

113.

Best, R.L., and C.C. Beegle. 1977. Food preferences of five species ofcarabids commonly found in Iowa cornfields. Envir. Ent. 6:912.

Bird, G.W., T. Eders, F.A. Drummond, and E. Groden. 1990. Design of

pest ma na gement systems for su staina ble agricultu re. In

Sustainable Agriculture in Temperate Zones, ed. C.A. Francis et

al. pp. 55110. John Wiley and Sons, Inc., New York.

Blum bur g, A.Y., and D.A. Crossley J r. 1983. Compa rison of soil

sur face a rt hr opod populat ions in convent iona l-tillage, no-tillage

and old-field systems. Agro-Ecosystem s 8:247253.

Boha rt , G.E., an d T.W. Koerber. 1972. Insects a nd seed pr oduction. In

S eed B iology, Vol 3, ed. T.T. Kozlowwski, pp. 150. AcademicPr ess, New York .

Boucher, D.H. 1981. Seed predation by mammals and forest

dominance by Quercus oleoides, a tr opical lowlan d oak. Oecologia

49:409414.


26/32


Briggs, J .B. 1965. Biology of some groun d beet les (Coleopt era :

Carabidae) injurious to strawberries. Bu ll. of En t. R es. 56:7993.

Bru st, G.E., an d G.J . House. 1987. Weed seed destr uction by

arthropods and rodents in low-input soybean agroecosystems.American J. Alternative Agriculture. 3(1):1925.

Car lson, E .C. 1967. Cont rol of sunflower m oth larva e an d t heir

dam age to sun flower seeds. J. Econ. Entomol. 60:10681071.

Charudattan, R., and C.J. Deloach. 1988. Management of pathogens

and insects for weed control in agroecosystems. In Weed

Man agem ent in A groecosystem s: Ecological Approaches, ed. M.M.

Altieri and M. Liebman, pp. 245264. CRC Press, Boca Raton, FL.

Chiverton, P.A. 1987. Predation ofRh opalosiphum padi (Homoptera:

Aphididae) by polyphagous predatory arthropods during the

aphids pre-peak period in spring barley. Ann. Appl. Biol. 111:257269.

Coaker, T.H., and A. Wiliams. 1963. The importance of some

Carabidae and Staphylinidae as predators of the cabbage root fly

Erioischia brassicae(Bouche). Entomologia Experimentalis et

Applicata 6:156164.

Connell, J.H. 1971. On the role of natural enemies in preventing

competitive exclusion in some marine animals and in rain forests.

In Dynamics of Populations, ed. P.J . den Boer an d G.R. Gra dwell,

pp. 298312. PUDOC, Wageningen.

Corn ic, J .F. 1973. Et ude du regime aliment aire de t rois especes decarabiques et de sez variations en verger de pomiers. An nals. S oc.

En t. Fr. 9:6987.

Crawley, M.J. 1992. Seed predators and plant population dynamics. In

S eeds, th e Ecology of R egeneration in Plan t Comm un ities, ed. M.

Fenner, pp. 157191. C.A.B. International, Wallingford, Oxon.

Cra wley, M.J ., and M.P. Gillma n. 1989. Population dyn am ics of

cinnabar moth and ragwort in grassland. J. Animal Ecology

58:10351050.

Culver, D.C., and A.J. Beattie. 1978. Myrmecochory in Viola: dynamics

of seed-an t int era ctions in some West Virginia species. J . Ecology66:6372.

Curtis, J. 1860. Farm Insects. Glasgow, Blackie.

Deloach, C.J. 1978. Considerations in introducting foreign biotic

agent s to cont rol nat ive weeds of ra ngeland s. Proc. 4th In t. Symp.

Biological Cont rol of Weeds, ed. T.E. Fr eema n. U niver sity of

Florida, Gainesville.

Dempst er, J . P. 1967. The cont rol ofPieris rapa ewith DDT I. The

natural mortality of the young stages ofPieris. J . Appl. Ecol.

4:485500.

DeSteven, D. 1983. Reproductive consequences of insect seedpredation in Hamamelis virginiana. Ecology 64 (1): 8998.

Duggan, A.E. 1985. Predispersal seed predation by Anthocharis

cardamines (Pieridae) in the population dynamics of the perennial

Cardam ine pra tensis (Brass.). Oikos 44:99106.


27/32


Forbes, S.A. 1880. Notes on insectivorous Coleopt era . Ill. State Lab.

Natur. Hist. Bull. 3:153160.

. 1883. The food relationships of Carabidae and Coccinellidae.

S tate Lab. Natu r. Hist. Bull. 1:3364.Forsyth e, S.F., an d A.K. Wat son. 1985. Predispersa l seed preda tion of

Canada thist le. Can. Ent. 117:10751081.

Franson, S.E., and M.F. Willson. 1983. Seed predation and patterns of

fruit production in Asclepias syriacaL. Oecologia 59:370376.

Gar dner , G. 1977. The r eproductive capacity ofFraxinus excelsioron

the Derbyshire lim estone. J . Ecology65:107118.

Goeden, R.D., and D.W. Ricker. 1985. Seasonal asynchrony of Italian

thistle, Cardu us pycnocepha lus, and the weevil Rhinocyllus

conicus (Coleopt era : Cur culionida e) int roduced for biological

control in Southern California. Environ. Entomol. 14:433436.Green T.W., and L.G. Palmbald. 1975. Effects of insect seed predators

on Astragalus cibariusand Astragalus uta bensis (Leguminosae).

Ecology 56:14351440.

Hainsworth, R.F., L.L. Wolf, and T. Mercier. 1984. Pollination and

pre-dispersal seed predation: Net effects on reproduction and

inflorescence characteristics in Ipomopsis aggregata. Oecologia

63:405409.

Hamon, N., R. Bardner, C. Allen-Williams, and J.B. Lee. 1990.

Car abid populat ions in field bean s an d th eir effect on t he

popula tion dyna mics ofS itona lineatus (L. ). An n. A ppl. Biol.117:5162.

Ha re, J .D. 1980. Var iat ion in fru it size and susceptibility to seed

predation among and within populations of the cocklebur,

Xanthium strum arium L. Oecologia 46:217222.

Ha rper , J .L. 1969. The r ole of predat ion in vegetat iona l diversit y.

Brookh aven S ym posia in Biology22:4862.

. 1977. The Population Biology of Plants. Academic Press,

London.

Harper, J.L., P.H. Lovell, and K.G. Moore. 1970. The shapes and sizes

of seeds. Annual Review Ecology and Systematics1:327356.Heithaus, E.R. 1981. Seed predation by rodents on three ant-dispersed

plants . Ecology 62:136145.

Holmes, P.M. 1990. Dispersa l an d pr edat ion in a lien Acacia. Oecologia

83:288290.

House, G.J., an d J .N. All. 1981. Car abid beetles in soybean

agroecosystems. Envir. Ent. 10:194196.

House, G.J., and R.W. Parmelee. 1985. Comparison of soil arthropods

and earthworms from conventional and no-tillage agroecosystems.

Soil Till. Res. 5:351360.

Hubbell, S.P. 1980. Seed predation and the coexistence of tree speciesin tropical forests. Oikos35:214229.

Imm s, A.D. 1948. A Gen eral T extbook of E nt om ology. E.D. Dutton and

Co., New York.

Inouye, R.S., G.S. Byers, and J.H. Brown. 1980. Effects of predation


28/32


and competition on survivorship, fecundity, and community

structure of desert annuals. Ecology 61 (6): 13441351.

J an zen, D. H. 1969. Seed-eat ers vs. seed size, num ber, toxicity, an d

dispersal. Evolution 23:127.. 1970. Herbivores and the number of tree species in tropical

forests. Am. Nat. 104:501528.

. 1971a. Seed predation by animals. Annual Review Ecology and

Systematics. 2:465492.

. 1971b. Sweep samples of tropical foliage insects: effects of

seasons, vegetation types, time of day, and insularity. Ecology

54:687708.

. 1972. Escape in space by S terculia apetalaseeds from the bug

Dysdercu fasciatus in a Costa Rican deciduous forest . Ecology.

53:350361.. 1980. Specificity of seed-at ta cking beet les in a Cost a Rican

deciduous forest. J . Ecology68:929952.

Johnson, N.E., and R.S. Cameron. 1969. Phytophagous ground beetles.

Annals Entomological Society of America62:909914.

J ulien, M.H. 1982. Biological Control of Weeds, A Catalogue of Agents

and Their Target Weeds. Commonwealth Agricultural Bureaux,

London.

Keeley, J.E., S.C. Keeley, C.C. Swift, and J. Lee. 1984. Seed predation

due to the Yucca-moth symbiosis. Am erican Midland N aturalist

112:187191.Kinsman, S., W. Platt, and J. Platt. 1984. The impact of a herbivore

upon Mirabilishirsuta, a fugitive prairie plant. Oecologia 65:26.

Kjellsson G. 1985. Seed fate in a population ofCarex pilu liferaL. II.

Seed predation and its consequences for dispersal and seed bank.

Oecologia 67:424429.

Koerber, T.W. 1962. Douglas fir cone and seed research. U.S . Forest

S ervice Pacific S outh west Forest Ran ge Exp erim ent al S tat ion

Progress Report 1959:137.

Kok, L.T., and R.L. Pienkowski. 1985. Biological control of musk

th istle by Rhinocyllus conicus(Coleoptera: Curculionidae) inVirgin ia from 1969 to 1980. Proc. VI In t. Sym p. Biological Cont rol

of Weeds, Vancouver, Canada, ed.E.S. Delfosse, pp. 805809.

Agric. Can .

Kok, L.T., and W.W. Surles. 1975. Successful biocontrol of musk

thistle by an introduced weevil, R hin ocyllus con icu. Environ.

Entomol. 4:10251027.

Kra ft, K.J . 1968. Ecology of th e cone moth Laspeyresia toreutain

Pinus banksianastands. An na ls En tom ological S ociety of Am erica

61:14621465.

Lam p, W.O., an d M.K. McCar ty. 1982. Pr edispersal seed p reda tion ofa native thistle, Cirsium can escens. Environ. Entomol. 11:847

851.

Leeuwen, B.H. van . 1983. The consequ ences of predat ion in t he

popula tion biology of th e m onocarp ic species Cirsium palustreand


29/32


Cirsium vulgare. Oecologia 58:178187.

Liebman, M., and R.R. Janke. 1990. Sustainable weed management

practices. In Sustainable Agriculture in Temperate Zones, ed. C.A.

Fr an cis et al., pp.111143. J ohn Wiley an d Sons, New York.Lipa, J .L. 1974. Sur vey and stu dy of insects a ssociat ed with

cruciferows plants in Poland and surrounding countries. Final

Rep. E21-ENT26-FG-PO-248, Inst. Plant Prot. Lab. Biol. Control

Miczurina 20, Poznan Poland.

Louda , S.M. 1978. A test of predispersal seed pr edat ion in t he

population dyn am ics of Haplopappu s (Aster aceae). Ph .D. Thesis,

Un iversity of Californ ia, Riverside a nd San Diego Stat e

University.

. 1982. Distribution ecology: variation in plant recruitment over

a gradient in relation to insect seed predation. EcologicalMonographs. 52 (1): 2541.

Louda, S.M., K.H. Keeler, and R.D. Holt. 1989. Herbivore influences

on plant performance and competitive interactions. In Perspectives

in Plant Competition, ed. J .B. Grace an d D. Tilma n. Academ ic

Pr ess, New York .

Luff, M. L. 1980. The biology of the ground beetle Harpalu s ru fipes in

a st rawberry field in N orth umberlan d. An n. A ppl. Biol. 94:153

164.

Lun d, R.D., an d F.T. Turpin. 1977. Car abid da ma ge to weed seeds

foun d in India na corn fields. Envir. Ent. 6:695698.Manley, G.V. 1992 Observations on Harpalu s pensylvanicus

(Coleoptera: Carabidae) in Michigan seed corn fields. Newsletter of

the Michigan Ent. Soc. 37 (4): 12.

Mares, M.A., and M.L. Rosenzweig. 1978. Granivory in North and

Sout h American desert s: rodents, birds, and a nt s. Ecology 59:235

241.

Mattson, W.J. 1971. Relationship between cone crop size and cone

damage by insects in red pine seed-production areas. Can. Ent.

103:617621.

McLemore, B.F. 1975. Cone and seed characteristics of fertilized andun fert ilized longleaf pines. USDA Forest Service Resear ch Pa per,

Southern Forest Experimental Station SO-109:110.

Merkel, E.P. 1967. Individua l slash pines differ in susceptibility t o

seedworm infestation. J. Forestry65: 32.

Miller, W. E. 1973. Insects a s r elated t o wood a nd nu t production. In

Black Walnu t as a Cr op. U.S. Forest Ser vice Genera l Techn ical

Report NC-4, Nort h Cent ra l Forest E xperiment Stat ion, St. Pau l,

MN.

Mittelbach, G.G., and K.L. Gross. 1984. Experimental studies of seed

predations in old-fields. Oecologia 65:713.Molau, U., B. Eriksen, and J.T. Knudsen. 1989. Predispersal seed

predation in Bartsia alpina. Oecologia 81:181185.

Moore, L.R. 1978. Seed predation in the legume Crotalaria. I.

Int ensity and variability of seed predation in na tive and


30/32


int roduced populat ions ofC. pallida Ait. Oecologia 34:185202.

Murdoch, W.W., F.C. Evans, and C.H. Peterson. 1972. Diversity and

pattern in plant s and insects . Ecology 53:819829.

Neser, S., and R.L. Kluge. 1985. A seed-feeding insects showingpromise in the control of a woody, invasive plant: the weevil

Erytenna consputaon Hakea seriea(Proteaceae) in South Africa.

Proc. VI Int. Symp. Biological Control Weeds, ed. E.S. Delfosse,

pp. 805809. Agricult ur e Can ada

Nielsen, S.G. 1977. Beech seeds as an ecosystem component. Oikos

29:268274.

Nilsson, S.G., an d U. Wast ljun g. 1987. Seed pr edat ion an d cross-

pollination in mastseeding beech (Fagus sylvatica) patches.

Ecology 68:260265.

Nitzsche, H. 1893. Ein neuer Fall von Saatlampbeschadigung durchLaufkafer Forst naturw. Zeitschr. 2 (48).

ODowd, D.J., and M.E. Hay. 1980. Mut ua lism between h ar vester a nt s

and a desert ephemeral: seed escape from rodents. Ecology

61:531540.

Pet ter sson, M.W. 1991. Flower h erbivory a nd seed preda tion in Silene

vulgaris (Caryophyllaceae): Effects of pollination and phenology.

Holarctic Ecology14(1):45-50.

Pimental, D. 1961. Species diversity and insect population outbreaks.

An na ls En tom ological Society Am erica54:7686.

Pr ice, W.P. 1984. Insect Ecology. John Wiley and Sons, New York.Pu rvis, G., an d J .P. Curr y. 1984. The influen ce of weeds an d farm yard

man ure on t he a ctivity of Cara bidae a nd th e groun d dwelling

ar th ropods in a sugar beet crop. J . Appl. Ecol. 21: 271283.

Randall, M.G.M. 1986. The predation of predispersed Juncus

squarrosusseeds by Coleophora alt icolella (Lepidopter a) la rvae

over a ran ge of altitu des in n ort hern En glan d. Oecologia 69:460

465.

Reader, R.J. 1993. Control of seedling emergence by ground cover and

seed predation in relation to seed size for some old-field species. J .

Ecology 81:169175.Risch, S., an d C.R. Car roll. 1986. Effects of seed pr eda tion by a

tr opical a nt on compet ition am ong weeds. Ecology 67(5): 1319

1327.

Rivar d, I. 1966. Ground beetles (Coleopter a: Car abidae) in r elation t o

agricultural crops. Can. Ent. 98:189195.

Robertson, A.I., R. Giddins, a nd T.J . Smith . 1990. Seed preda tion by

insects in t ropical m an grove forest s: exten t an d effects on seed

viability a nd th e growth of seedlings. Oecologia 83:213219.

Rosentha l, S.S. 1985. Poten tia l for biological contr ol of field bindweed

in Ca lifornia s coast al vineya rds. Agric. Ecosyst En viron. 13:43-57.

Rosenthal, S.S., and G.R. Buckingham. 1982. Natural enemies of

Convolvulu s arvensis in western Mediterranean Europe.

Hilgardia 50:126.


31/32


Sallaba nk s, R., and S.P. Cour tn ey. 1992. Fr ugivory, seed preda tion,

an d insect-vertebrat e int eractions. Annual Review Entomology

37:377400.

Salisbury, E.J. 1942. The Reproductive Capacity of Plants. Bell,London.

Scherney, F. 1960. Kartoffel kaferbekampfung mit laufkafern

(Gattung Carabus). Pflanzenchutz 12:3435.

Schupp, E.W. 1988. Factors affecting post-dispersal seed survival in a

tropical forest. Oecologia 76:525530.

Sheppa rd, A.W. 1987. Insect her bivore compet ition an d t he popula tion

dynamics ofHeracleum sphond ylium L. (Umbelliferae). Ph.D.

thesis, University of London.

Silvertown, J .W. 1980. The evolut iona ry ecology of mas t seedling in

trees. Biological J . Lin nean S ociety14:235250.Skuhravy, V. 1959. Die nahrung der Feldcarabiden. Acta. Soc. Ent.

Cechoslov. 56(1): 118.

Smith , C.C. 1975. The coevolut ion of plan ts an d seed pr edat ors. In

Coevolution of Animals and Plants, ed. L.E. Gilberg and P.H.

Raven. Un iversity of Texas Pr ess, Aust in.

Solbreck, C., and B. Sillen-Tullberg. 1986. Seed production and seed

predation in a patchy and time-varying environment. Dynamics of

a milkweed-tephritid fly system. Oecologia 71:5158.

Speight, M.R., and J.H. Lawton. 1976. The influence of weed-cover on

the mortality imposed on artificial prey by predatory groundbeetles in cereal fields. Oecologia 23:211223.

Sun derlan d, K.D. 1975. The diet of some pr edat ory a rt hr opods in

cereal crops. J . Applied E cology12:507515.

Sunderland, K.D., N.E. Crook, D.L. Stacey, and B.J. Fuller. 1987. A

stu dy of feeding by polypha gous preda tors on cereal aph ids using

ELISA and gut dissection. J. Applied Ecology24:907933.

Thiele, H.U. 1964. Experimentelle untersuchungen uber die ursache

der biotopbindung bei Carabiden. Zeitschriftfur Morphologie

Okologie der Tiere. 53:387452.

. 1977. Carabid Beetles in Their Environments, A Study onHabitat S election by Ad aptations in Physiology and Behaviour.

Springer-Verlag, New York.

Traveset, A. 1990. Post-dispersal predation ofAcacia farn esian a seeds

by S tator vachelliae(Bruchidae) in Central America. Oecologia

84:506512.

. 1991. Pre-dispersa l seed pr edat ion in Cen tr al American Acacia

farnesiana: factors affecting the abundance of co-occurring bruchid

beetles. Oecologia 87:570576.

Webster, F.M. 1880. Notes upon the food of predaceous beetles. Ill.

S tate Lab. Natu r. Hist. Bull. 3:149152.. 1900. Harpalus caliginosusas a stra wberry pest with n otes on

oth er ph ytopha gous Cara bidae. Can. Ent. 32:265271.

Werner, R.S. 1964. White spru ce seed loss caused by insects in in ter ior

Alaska. Can. Ent. 96:14621464.


32/32


Whelan, C.J., M.F. Willson, C.A. Tuma, and I. Souza-Pinto. 1990.

Spatial a nd temporal pat tern s of postdispersal seed predat ion.

Can. J. Bot. 69:428436.

Willson, M.F. 1983. Natural history ofActaea ru bra: fruit dimorphismand fruit/seed predation. Bulletin Torrey Botanical Club. 110:298

303.

. 1992. The ecology of seed dispersal. In S eed s, th e Ecology of

R egeneration in Plant Com m un ities, ed. M. Fenner. CAB

International, Oxford.

Wilson, D.E., an d D.H. J an zen. 1972. Preda tion on Scheelea palm

seeds by bruchid beetles: seed density and distance from the

parent palm. Ecology 53:954959.

Zha ng, J . 1993. Biology ofHarpalu s ru fipes DeGeer (Coleoptera:

Carabidae) in Maine and dynamics of seed predation. M.S. thesis,University of Maine, Orono.

Zhang, J., F. Drummond, and M. Liebman. 1994. Spread ofHarpalus

rufipesDeGeer (Coleoptera : Cara bidae) in eastern Cana da an d t he

United States . En tom ol. Trend s in Agric. S ci. 2:6771.

Znam ens kii, A.V. 1926. In sects inju rious to agricultu re. I. Pests of

grain crops. Trud. Poltavsk. Sel. Khoz. Op. Stants, no. 50.

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Insect Predation of Seeds and Plant Populations Dynamics