Alphey, T.J.W.

Boag, B.

Name not available

Influence of interspecific competition on the population dynamics of migratory plant-parasitic nematodes with r and K survival strategies

Horizon / Pleins textes

Influence of interspecific competition on  the  population 
dynamics of migratory plant-parasitic nematodes 
with r and K survival  strategies 
Brian BOAG and Thomas J. W. ALPHEY 
Scottish Crop Research Institute, Invergowrie, 
Dundee DD2 5DA, U.K. 
SUMMARY 
Samples taken over a five year period at a field site in which the dominant plant-parasitic nematode species were Rotylenchzls 
robustus, Trichodorus primnitivus and ParatricRodorus.pachydemzus indicated that the  nematodes  had IZ survival  strategies.  They 
had  relatively  low  rates  of  multiplication  and  their  numbers  showed  no  obvious  seasonal  cycling. In soil  where their  numbers  had 
been  greatly  reduced  following  treatment  with  the  fumigant  dichloropropene,  numbers  of  a  fourth  species Paratylenchus nanus, 
initially  present  in  small  numbers,  rapidly  increased. This species  had an r  survival  strategy,  its  numbers  increasing  rapidly in the 
absence  of  competition and also  showing  marked  seasonal  fluctuations. In non-fumigated  soil P. nanus numbers  remained  low, 
probably  due to interspecific  competition,  especially  with R. robustus. 
RESUME 
Injluence de la compétition  interspécifque sur la dynamique des populations de nématodes phytoparasites migrateurs 
ayant des stratégies de survie de types (( r )> et (( I< N 
Des  prélèvements  effectués  pendant  cinq  années  dans un champ où les  espèces  dominantes  de  nématodes  phytoparasites  étaient 
Rotylenchus robustus, Trichodorus primitivus et Paratrichodorus pachydenms, permettent  d’attribuer à ces  nématodes une  stratégie 
de survie de type (( I< n. Leur taux de multiplication  est  relativement  faible et ils  ne  montrent  pas  de cycle  saisonnier net.  Dans 
les  sols où les  populations  de  ces  nématodes  ont  été  drastiquement  réduites  par  application  d’un  nématicide  fumigant  (dichloro- 
propène),  une  quatrième  espèce, Paratylenchus nanus, voit  son  taux,  initialement  faible,  croître  rapidement.  Cette  espèce  a une 
stratégie  de  survie  de  type (( r D, le  nombre  de  ses  individus  croissant  rapidement  en  l’absence  de  compétition et les  fluctuations 
saisonnières  de  sa  population  étant  bien  marquées.  Dans  les  sols  non  traités  avec un nématicide  fumigant,  le  taux  de P. nanus reste 
faible,  ceci  étant  probablement dû à la  compétition  interspécifique, R. robustus semblant  plus  particulièrement en cause. 
The role of competition in limiting  insect  and  mam- 
mal populations is well documented  but its  influence in 
regulating  nematode  populations  has received little 
attention  and is less well understood. Boag (1986) 
demonstrated that intraspecific  competition  limited the 
maximum population density of Rotylenchus robustus 
populations under perennial  crops  and  Seinhorst (1965) 
developed his yield response curves from the compe- 
tition models of Nicholson (1933). Interspecific com- 
petition  has  been  demonstrated  under  laboratory  con- 
ditions  (Johnson,  1970;  IGaus-Schmidt & Lewis, 1981) 
but there are few examples recorded from field situ- 
ations (Bird, Brooks & Perry, 1974). The population 
dynamics of competing parasitic animals has recently 
been reviewed (Dobson,  1985) and Adamson (1985) has 
commented upon  the r  and I< strategies of nematode 
parasites of millipedes. In this  paper  the  effect of inter- 
specific  competition on field  populations  and the  sur- 
vival strategies of the plant parasitic  nematodes R. 
robustus,  Trichodorus  primitivus,  Paratrichodorus pa- 
chydernzus and Paratylenchus  nanus are  reported. 
Revue Nématol. I I  (3) : 321-326 (1988) 
Materials and  methods 
The data  in  this  paper  are  from  a  series of ecological 
studies which examined the effect of different  host  crops 
on  the  population dynamics of R. robustus and trichodo- 
rid  nematodes at a  Scottish  forest  nursery site. Details 
of the experimental  design and  procedure have already 
been  published (Alphey, 1985; Boag, 1986). At the site 
one half of each  experimental  plot was fumigated  with 
dichloropropene (92 % a.i. as Telone 11) at 207 llha 
applied  by  hand  injector gun at a depth of 20 cm. The 
other half of each  plot was untreated.  After  four weeks 
and aeration by rotary  cultivation,  each  plot was sown 
with perennial ryegrasslwhite clover (Lolium perennel  
Trifolium  repens) mixture. 
Composite soil samples were taken at various  depths 
(Tab. 2 )  every two months  between May 1980 and  July 
1985. Sampling  points were marked to avoid resampling. 
After mixing, 200 g subsamples were soaked in water 
overnight (Simons, 1973) and nematodes  extracted 
using  a  modified  sieving and  decanting technique,  heat 
32 1 
B. Broag di T. J. W! Alphey 
20 
O 
90 
O 
30 r 0-9cm 
30 r 20-29 
30 r 30-39 
3o r 40-49 t- 1 
0 1  1 I I 1 I 1 I 1 
1980  1981  1982  1983  1984  1985 
Fig. 1. Temperature  and  rainfall  measurements  from the Scottish  Crop  Research  Institute,  Invergowrie  and  percentage soi1 moisture 
content  from  samples  taken  under  grass/clover  sward at the forest  nursery. 
322 Revue Nématol. II (3) : 321-326 (1988) 
Migrato y plant-parasitic nematodes; r and I< survival strategies 
8oo r 
O 
80 r; 
- .- 
O 
v) 
f 40 
U 
O 
cn 
O 
Cu 
50 
O 
O 
Paratrichodorus  pachydermus 
800 
400 
O 
1980  1981  1982  1983  1984  1985 
Fig. 2. Variation in mean  nematode  numbers (0,50 cm)  May 1980 to May 1985, O, fumigated; @, non-fumigated. 
Revue Neinatol. 11 (3) : 321-326 (1988) 323 
B. Broag di T. J. W. Alphey 
killed, fixed, stored and  counted as described by Boag 
(1974). Nematodes  expressed as numbers  per 200 g  dry 
soil were transformed to (x + 1)  for  statistical analysis, 
Observations showed that meteorological  data  period- 
ically recorded at  the nursery was very similar  to that 
routinely  recorded at the meteorological  site of the 
Scottish  Crop  Research  Institute (Boag, 1982) and 
consequently the latter  data  are  used in this  paper. 
The occurrence of nematophagous  fungi, which may 
have limited nematode populations was tested for in 
1984 using the soil sprinkling technique described by 
Duddington (1955). Panagrelltu  redivivus was used 
3s the target organism because it has been shown to 
stimulate  the  predatory  activity of a wide range of nema- 
tophagous  fungi  (Jansson & Norbring-Hertz, 1980). 
Preliminary  identification of the  fungi  found was 
made using  the key  of Cooke and Godfrey (1964) and 
subsequently confirmation was made by staff at the 
Commonwealth  Mycological  Institute, Kew. 
Results 
Between  1980 and 1985 there was no consistent  season- 
al pattern in the monthly ramfall data but seasonal 
fluctuations in temperature and percentage soil mois- 
ture  content were observed. Low soil moisture levels, of 
8 O/O (pF 3.8) (Boag, 1982) in  July  1982  and  July 1984 
and surface  temperatures below - 230 in January 1982 
did not decrease the  numbers  recovered of any of the 
nematode species under  study (Figs 1 & 2). 
- 
Prior to  fumigation  in 1980 the  most abundant 
plant-parasitic  species were R. robustus (229/200 g soil), 
T. primitivus (31/200  g soil) and Paratrichodorus pachy- 
demzus (14/200 g soil). Paratylenchus nanus was ex- 
tremely  scarce (< 0.2/200  g soil). Subsequently the 
grass mixture was shown to be a good host for R. 
robustus, T. primitivus and P. pachydermms, their num- 
bers progressively increasing over the  first 2-3 years in 
the non-fumigated subplots (Fig. 2). Although their 
numbers  declined  later,  they were  still greater  after  five 
years than  at  the  start of the experiment in  May 1980 
(Tab. 1). Dichloropropene reduced the numbers of R. 
robustus, T. primitivus and P. pachydermus by 94-96 Yo 
between May  and  July 1980 (Fig. 2). The small residual 
populations  urvived and increased  throughout  he 
duration of the experiment but their annual rate of 
increase was small and never exceeded x 2.25 (Tab. 1). 
Consequently, after five years the populations of R. 
robustus and Paratrichodorus pachydermtls hed  still not 
attained the initial 1980 population levels. 
The population  density of Paratylenchus nanus at  the 
site was initially very low and was further  decreased to 
below the detectable level by fumigation. It was not  until 
1982 that the species was again detected in al1 plots. 
Numbers of P. nanus increased  little in  the  non-fumi- 
gated  plots whereas in  the fumigated  plots  they  increas- 
ed  rapidly. In  the  first two years following fumigation 
annual  multiplication  rates were c. x 7 and x 184 
(Tab.  1).  Numbers of P. nanus also exhibited marked 
seasonal fluctuations with the highest numbers being 
recorded in  the  autumn  and  the lowest numbers  in  early 
spring. 
Table  1 
Comparison  of the  rates of multiplication of Rotylenchus robustus,  Trichodorus primitivus, 
Paratrichodorus  pachydemzus and Paratylenchus  nanzls in  fumigated  and  non-fumigated  plots  growing 
gass berneen May 1980-May 1985 (mean numbers of nematodes 200 g dry soil, depth 0-50 cm) 
(Figures in parenthesis  refer to mean  yearly  percentage  population  increases  or  decreases  over  that of the  previous  year) 
Date R. robustus T. primitivus P. pachydermus P. nanus 
Non Non Non Non 
Fumigated Ftrmigated Fumigated  Fumigated Funligated Fumigated Fumigated Fumigated 
Initial population 
May 1980 226 23 1 21 40 12 15 o. 1 
July 1980-May 1981 13 (- 94) 180 (- 22)  .0 (- 95) 41 (3) 0.5 (- 95) 11 (- 27) 0.8 (700) 3.3 (1 550) 
July 1981-May  1982"' 37 (185) 404 (124) 6.5 (225) 58 (41) 1.0 (100) ~ 16 (45) 148  (18 400) 25 (658) 
July 1982-May  1983*  76 (105) 587 (45) 14  (115)67 (16) 1.8 (80) 25 (56) 446  (101) 37 (48) 
July 1983-May 1984g 103 (36) 482 (- 18) 25 (79) 40 (- 41) 4.5 (150) 36 (44) 360 (- 19) 31 (- 16) 
July 1984-May 1985" 160 (55) 467 (- 3) 31 (24) 40 (0) 7.5 (67) 32 (- 11) 601 (67) 75 (142) 
Overall effect** 1 131 159 1  450 . - 2  1 500 191 75 025 2 170 
0.2 
* Yearly counts comprise mean  counts  for July, September, November, January, March  and May. 
** Overall effect refers to  the percentage population increase or decrease between the year of July 1980-May 1981 and July 1984-May 1985. 
324 Revue Niinatol. 11 (3) : 321-326 (19881 
Migrato y plant-parasitic nematodes; r and I< survival strategies 
A study of the  depth distribution of the  four species 
indicated that T. prinzitivus and Paratrichodorus pachy- 
dennus were generally found  at greater  depths than R. 
robustus and Paratylenchus  nanus which were more 
abundant  in  the  top 20 cm of soil (Tab. 2). The  depth 
distribution of the two  trichodorid species were signifi- 
cantly  correlated ( r  = 0.946, D. F. = 3) and that 
between R. robustus and P. nanus was highly significant 
( r  = 0.979, D. F. = 3). 
Table  2 
Depth  distribution of Rotylenclzus robustus, 
Trichodorus primitivus, Paratrichodorus pachydemzus 
and Paratylenchus nanus [mean nematode numbers (May 
1980-May 1985)/200 g dry  soil] 
Depth R. robus- T. primi- P. pachy- P. nanus 
icnz) tus tiVUS dermus 
0-9  435(35) * 36  (22) 16  (23)  21  (38) 
10-19 384(31) 42  (26) 18  (26) 316  (38) 
20-29 226(18) 42(26) 19(28) 138(17) 
30-39 126(10) 26(16) lO(14) 37  (4) 
40-49 79  (6) 17(10) 6  (9) 25 (3) 
* Figures in parenthesis refer to the percentage of the nematodes 
found at that depth. 
Two nematophagous fungi, Arthrobotrys oligospora 
(Frss.), and Monaerosporium bembicoides (Drechsler) 
were detected at  the site. The  fungi were found  in  both 
fumigated  and  non-fumigated  sub-plots  in  May 1984. 
Discussion 
The factors responsible for the marked increase in 
numbers of P. nanus in the dichloropropene treated 
sub-plots and  not  in  the  untreated sub-plots  are not fully 
understood. There is no evidence  to  suggest  differential 
susceptibiity of any of the nematode species to dichloro- 
propene. Dichloropropene has some fungicidal action 
(Buczacki & White,  1979) and initially it was suspected 
that it may have reduced the population of nemato- 
phagous fungi  thereby allowing the residual  populations 
of P. nanus to increase. However, this is  now considered 
unlikely as both A. oligospora and M. bembicoides were 
detected from  the  fumigated as well as the non-fumi- 
gated sub-plots. If nematophagous fungi had been a 
major predator  limiting  populations of P. nanm then a 
marked  decrease in  the  nematode  numbers would have 
been  expected  as the fumigated  plots  became recolonis- 
ed by fungi. However, there was no evidence of this 
occurring. The  depth distribution of P. nanus and of 
R. robustus were similar and  the crops grass and clover 
are  known to be  a ,good hosts for  both  nematode  species 
Revue Nénzatol. 11 (3) : 321-326 (1988) 
(Rossner, 1971; Coursen,  Rohde & Jenkins, 1958). 
Furthermore,  studies  using  plants  growing  in  agar 
(Rhoades & Linford, 1961; Klinkenberg, 1963; Boag, 
1980) have shown that both these species feed in a 
similar  manner  ectoparasitically on  the root  epidermis 
and  root  hairs.  Therefore,  although it  cannot  be  proved 
it seems probable that competition between the two 
species, occupying similar ecological niches, was the 
main  factor  preventing  numbers of P. nanus increasing 
in  the non-fumigated  sub-plots.  Once  competition from 
R. robustus had been removed in the fumigated sub- 
plots P. nanus numbers  increased rapidly. The density 
of P. nanus population in the fumigated plots was 
probably  regulated by seasonal  variation in  the availa- 
bility of food and by intraspecific  competition. 
This  study also demonstrated the difference in  sur- 
vival strategies of the nematode  species. Two types of 
survival strategies in animals have been described by 
Southwood (1981). I< strategists tend  to be  large  animals 
with slow multiplication  rates and are not readily able to 
exploit  changes in environmental  conditions. In contrast 
r strategists are small animals with fast multiplication 
rates giving them the ability to rapidly colonise and 
exploit new favourable environments. R. robustus, T. 
primitivus and ?aratrichodorus pachydennus had rela- 
tively low rates of multiplication, even when initial 
populations were small. Under Scottish  conditions, the 
low rates of multiplication, relative stability in popu- 
lation  infrastructures  and lack of any  marked  seasonal 
fluctuation of numbers of these nematodes (Bocg, 1981; 
Boag, 1982; Alphey, 1985)  are  characteristics  which 
identify  them as K survival strategists. These character- 
istics  contrast  strongly  with  those of Paratylench,us 
nanus a  nematode which, when  competition was reduc- 
ed,  exhibited  high  multiplication  rates  and  marked 
seasonal fluctuations in its numbers - the character- 
istics of an organism  with  a  r  survival  strategy. In  the 
non-fumigated sub-plots numbers of P. nanus were 
suppressed  and  remained low due  to interspecific  com- 
petition from  the many R. robustus which  acted in  an 
imperfectly  density-dependent manner (Milne, 1984). 
These results show that  fumigant nematicides,  such 
as dichloropropene, can give long-term control of I< 
survival strategy nematodes, but that these chemicals 
can  also allow other  pathogenic  species  with  r  survival 
strategies  such as P. nanus (Winfield, 1985) to multiply 
rapidly. 
REFERENCES 
ADAMSON, M. L. (1985).  Rhizonematida  (Nematoda) of Rlti- 
nocricus benlardinensis (Rhinocricidae;  Spriobolida;  Diplo- 
poda) with comments on r- and K-selection in nematode 
parasties of diploids. Revue Suisse Zool,, 92 : 871-896. 
ALPHEY, T. J. W. (1985).  A  study of spatial  distribution  and 
population  dynamics of two sympatric  species of trichodorid 
nematodes. Am. appl. Biol. 107 : 497-509. 
305 
B. Broag di T. J. W: Alphey 
BIRD, G. W.,  BROOKS, O. L. & PERRY,  C.E.  (1974).  Dynamics 
of  concomitant  field  populations  of Hoplolaimus columbzls 
and fileloidogyne  incognita. J. Nematol, 6 : 190-194. 
BOAG,  B.  (1974).  Nematodes  associated with forest  and  wood- 
land  trees in Scotland. Ann. appl. Biol., 77 : 41-50. 
BOAG, B. (1980). Observations of temperature on rates of 
feeding of the plant-parasitic  nematodes Rotylenchus robzcs- 
tus, Xiphinema diversicaudatum and Hemicycliophora 
conida. J .  Nematol., 12 : 193-195. 
BOAG, B. (1981). Observations on the population dynamics 
and vertical distribution of trichodorid nematodes in a 
Scottish  forest  nursery. Ann. appl. Biol., 98 : 463-469. 
BOAG, B. (1982). Observations on the population dynamics, 
life  cycle and ecology of the  plant-parasitic  nematode Ro- 
tylenchzls robustus. Ann. appl. Biol., 100 : 157-165. 
BOAG, B. (1986). The influence of host and intra-specific 
competition in controlling  populations  of the plant  parasitic 
nematode Rotylenchus robustus (Nematoda : Hoplolaimi- 
dae). Nematologica, 31 (1985) : 344-351. 
BUCZACKI, S .  T. & WHITE, J. G. (1979). The value of soil 
sterilants for the control of clubroot on a field scale. Pl. 
Path., 28 : 36-39. 
COOICE,  R. C. & GODFREY,  B.E.S.  (1964).  A  key to the nema- 
tode  destroying  fungi. Trans. Br. mycol. Soc., 34 : 322-331. 
COURSEN, B. W., ROHDE, R. A. & JENICINS, W. R. (1958). 
Additions  to  the  host  lists of the  nematodes Paratylenchus 
profectus and Trichodorus christiei. Pl. Dis.  Reptr, 42 : 
DOBSON, A. P. (1985). The population  dynamics of competi- 
tion  between  parasites. Parasitology, 91 : 317-347. 
DUDDINGTON, C. L. (1985).  Notes  on  the  technique  of  hand- 
ling predaceous fungi. Trans. Br. mycol. Soc., 38 : 97-103. 
JANSSON, H. B. & NORDBRING-HERTZ, B. (1980). Interaction 
between nematophagous fungi and plant-parasitic nema- 
todes : attraction,  induction  of  trap  formation  and  capture. 
Nematologica, 26 : 383-389. 
456-460. 
JOHNSON, A.  M.  (1970).  Pathogenicity and  interaction  of  three 
nematode  species  and six Bermuda  grasses. J. Nematol., 2 : 
KLINKENBERG, C. H. (1963). Observations on the feeding 
habits of Rotylenchus robustus, Pratylenchus crenatzls, P. 
penetrans,  Tylenchorhynchus dubius and Hemicyliophora 
similis. Nematologica, 9 : 502-506. 
KRAUS-SCHMIDT, H. & LEWIS, S .  A. (1981). Dynamics of 
concomitant  populations  of Hopblaimzu columbzls, Scutel- 
lonema  brachyvrum and Meloidoygne  incognita on Cotton. 
J. Nematol., 13 : 41-48. 
MILNE, A.  (1984).  Fluctuations and natural  control  of  animal 
populations,  as  exemplified in the garden  chafer Phylloper- 
tha horticola (L.). Proc. Roy. Soc. Edinburg, 82  B : 145-199. 
NICHOLSON,  A.  J.  (1933). The balance  of  animal  populations 
J.  Anim. Ecol., 2 : 132-178. 
RHOADES, H. L. & LINFORD, M. B. (1961). A study of the 
parasitic habit of Paratylenchus projectus and P. dianthus. 
Proc. helminth. Soc. Wash., 28 : 185-190. 
ROSSNER, J. (1971). Untersuchungen zur Entwicklung von 
Rotylenchus robustus. Nematologica, 17 : 255-261. 
SEINHORST, J. W.  (1965). The relationship  between  nematode 
density  and  damage to plants. Nematologica, 11 : 137-154. 
SIMONS, W. R. (1973). Nematode survival in relation to soil 
moisture. Meded. LandbouwHogesch., Wageningen, 73 : 
SOUTHWOOD, T. R. E. (1981).  Bionomic  strategies  and  popula- 
tion  parameters. In : May,  R. M. (Ed.). Theoretical  ecology, 
principles  and  applications, Oxford,  Blackwell  Scientific 
Publications : 30-52. 
WINFIELD, A. L. (1985). Observations on the pin nematode 
Paratylenchus nanus, a possible pest of glasshouse lettuce 
Lactuca  sativa. Crop Res., 25 : 3-12. 
36-41. 
1-85. 
Accepté pozw publication le 17 aozit 1987. 
326 Revue Nématol. I I  (3) : 321-326 (1988) 


Influence of interspecific competition on the population dynamics of migratory plant-parasitic nematodes with r and K survival strategies

Abstract

Similar works

Full text

Available Versions

Name not available

Horizon / Pleins textes