Tylenchidae (Filipjev, 1934)

Sigareva, D. D., Fedorenko, S. V., Bondar, T. I., Sokolova, O. O. & Kornyushin, V. V., 2019, Communities Of Ditylenchus Destructor Satellite Species Of Nematodes In Infected Potato Tubers: Species Composition Of Phytonematode Complex And The Structure Of Their Infracommunities, Vestnik Zoologii 53 (6), pp. 443-458 : 447-454

Order Tylenchidae (Filipjev, 1934)

Family Anguinidae Nicoll, 1935

Genus Ditylenchus Filipjev, 1934

Ditylenchus destructor Thorne, 1945

Family Tylenchidae Oerley, 1880

Genus Aglenchus (Andrassy, 1954)

Aglenchus agricola (de Man, 1834) Andrassy, 1954

Family Neotylenchidae Thorne, 1941

Genus Nothotylenchus Thorne, 1941

Nothotylenchus sp.

Family Aphelenchidae (Fuchs, 1937)

Genus Aphelenchus Bastian, 1965

Aphelenchus avenae Bastian, 1965

Family Aphelenchoididae (Skarbilovich, 1947)

Genus Aphelenchoides Fischer, 1894

Aphelenchoides asterocaudatus Das, 1960

Aphelenchoides bicaudatus (Immamura, 1931) Filipjev et Sch. Stekhoven, 1941 Aphelenchoides limberi Steiner, 1936

Within the order Tylenchida four family are distinguished: Anguinidae , Tylenchidae and Aphelenchidae , Aphelenchoididae of which Anguinidae is represented by phytohelminths and three other mycohelmints.

The order Rhabditida consists of four families: Diplogasteroididae , Cephalobidae , Rhabditidae and Panogrolaimidae, represented exclusively by saprobiotic species. Family Diplogasteroididae contains only one genus Diplogaster . The Cephalobidae family contains four genera: the Cephalobus , Eucephalobus , Acrobeloides and Chiloplacus . The Rabditidae contains four genera too: Cenorhabditis, Mesorhabditis , Rhabditis and Pelodera . The Panogrolaimoides family contains only one genus Panogrolaimus. Most (13 of 15) genera are also represented by one species (9), the genus Eucephalobus — by two species, and only the genus Aphelenchoides includes three species (fig. 2, A).

Diplogasteroididae ; 1

Phytonemat; 1

; 3

Cephalobidae

Anguinidae ; 1

Mycohelminths; 6

Tylenchidae ; 1

; 1

Rhabditidae

; 1

A Panogrolaimida; 1 B Saprobionts; 11

Fig. 2. Structure of phytonematode communities inhabiting tubers damaged by D. destructor (A — taxonomic structure, B — ecotrophic structure).

Along with D. destructor , which is a pathogenic phytohelminth and an edificator species, two more ecotrophic groups of nematode satellites of Ditylenhus are included in the community of phytonematodes, inhabiting the lesion site caused by ditylenchosis that occur in potato tubers during storage in winter storage facilities (fig. 2, B). Representatives of mycohelminths settle in potatoes affected by D. destructor because this species destroys the living tissues of tubers in the course of life, creating favorable conditions for the settlement of certain species of fungi. It is the colony of these fungi consumed by mycohelminths nematodes. Such species are six in four genera. Aphelenchoides asterocaudatus and Aph. limberi predominate in frequency and number of infrapopulations (table 1).

Representatives of ecotrophic groups of nematodes appear in the affected tubers already in the first stage of the course of the disease ( fig. 3 ).

Representatives of the second ecotrophic group of saprobiont nematodes are found in the areas of ditylenchosis lesion of potato tubers a little later, when the part of the cells of the potato parenchyma is destroyed and the fungi are joined by saprobiotic microorganisms, and saprobiont nematodes feed on them. This ecotrophic group of nematodes is more diverse, with 11 species from 10 genera. Three species Mesorhabditis monhystera , Acrobeloides buetschlii , and Chiloplacus simmetricus predominate in frequency of occurrence and population size (table 1).

In general, the taxonomic structure of the phytonematode complex, which is formed in the affected by D. destructor potato tubers under conditions of preservation in the storage of the Institute of Potato Production of NAAS of Ukraine, consists of five groups, which are determined by quantitative indicators ( fig. 4).

According to the method of tuber selection for the study, potatoes infected only with D. destructor were included into the common sample. Therefore, the intensity of infestation by this species of nematodes, which is an edificator for the phytonematode satellite community, is a priori absolute (100 %). D. destructor is a dominant phytonematode in this community. However, the infestation rate of this species (number of infrapopulations) in one tuber varies widely from 1 specimen to 2,128 –5,235 specimens, with an average infection (I) of 282 specimens, which is quite high. In addition, in 4 cases of the studied tubers only D. destructor was detected in the absence of any nematode satellite species.

The group of subdominant species is quite large, with four species (P 30–50 %). Two species of mycohelminths Aphelenchoides asterocaudatus and Aphelenchoides limbery and two species of saprobionts Mesorhabditis monhystera and Acrobeloides buetschlii are among them. The intensity of infection is usually average, although it can reach very high values — 397 (up to 1260–3144) specimens of Aphelenchoides limbery . At the same time, Mesorhabditis monhystera is relatively small in number — 9 (1–67) specimens.

Slightly smaller is the group of common species (P 10–30 %), which includes only 3 species, one species of the mycohelminthic Aphelenchus avenae , which is small in number, 10 (1–50). Of two species of saprobiont nematodes, one Chiloplacus simmetricus has an average abundance I of 52 (1–219) specimens, while the abundance of the other species, Diploscapter rizophilus , is very low — I only 3 (1–7) specimens.

All other D. destructor satellite phytonematodes were not common. These ten species were found 1–3 times (P 2.33–6.98 %) and, accordingly, they are classified as rare. However, the various species of this group differ significantly from each other in terms of the number of infrapopulations. A significant part of rare species has an average level of abundance (23– 71 specimens). In particular, these are all three species of mycohelminths assigned to this group ( Aphelenchoides bicaudatus , Aglenchus agricola and Nothotylenchus sp. ), as well as Eucephalobus oxiuroides from saprobionts. Two more species of saprobionts are distinguished by high ( Rhabditis sp. — 257 specimens) and ultrahigh ( Caenorhabditis elegans — 1444 specimens) numbers in the affected tubers. Probably, their rare occurrence in our samples is due to some external factors for the system. The remaining four species of saprobionts ( Pelodera teres , Eucephalobus mucronatus , Panagrolaimus rigidus and Cephalobus persegnis ) were found 1–2 times in an amount of less than 10 specimens. They can be considered random components of the D. destructor satellite nematode community.

In general, subdominant species make up 23.53 % of all 17 D. destructor satellite species. Common species make up another 17.65 %, while rare species make up 58.83 %, of which 23.53 % are accidental species. The specific frequency of occurrence is repeated for two pairs (14 and 7 times), 4 species were found 4 times and 3 and 2 species were recorded 3 times ( fig. 4).

Tubers occupancy by phytonematodes at different stages of the course of the disease.

According to the nature of the development of the potato tubers disease, most authors ( Paramonov, Bryushkova, 1956; Zhilina, 2004, and others) divide it into 5 main stages, taking into account the appearance of diseased tubers and the cells occupancy by various groups of phytonematodes: phytohelminths, mycohelminths, and saprobionts (table 2). We took the same approach. At stage I of the disease, the tubers are almost no different from healthy ones; in the affected tissues, D. destructor is in small amounts (10 specimens per 10 g of tissue) as well as mycohelminthics, namely Aphelenchoides asterocaudatus (35 specimens) and Aglenchus agricola (10 specimens in 10 g of tissue). At stages II and III of the disease, the number of potato rot nematodes increases sharply (up to 435 and 540 specimens per 10 g of tissue). At the same time tubers are being populated by mycohelminths (up to 40 and 320 specimens in 10 g of tissue) and saprobionts (41 and 67 specimens in 10 g of tissue). At these stages, Aphelenchoides asterocaudatus and Aphelenchoides limberi (76 and 226 specimens per 10 g of tissue) reached the highest numbers among mycohelminths, Acrobeloides buetschlii (52 specimens) and Chiloplacus symmetricus (22 specimens per 10 g of tissue) among saprobionts.

The abundance of D. destructor peaks at stage III of the the disease, as well as the number of mycohelminths (320 and 1540 per potato on average, 4 species), but the maximum number of saprobionts (439, 9 species) occurs at stage V of the disease. At the same time, the number of D. destructor is only 77 in one tuber.

Thus, the IV–V stages of ditylenchosis are accompanied by changing the number of phytonematode species and their abundance in favor of saprobionts and mycohelminths. The number of D. destructor , respectively, is 52– 77 specimens per 10 g of tuber, and the number of mycohelminthes and saprobionts remains high and even increases (table 2). At these stages of the disease, the most prevalent species among mycohelminths are Aphelenchoides limberi — (14 affected tubers), Aphelenchoides asterocaudatus — 19 affected tubers out of 43, and saprobionts — Caenorhabditis elegans , Chiloplacus symmetricus (11 affected tubers), Acrobeloides buetschlii (14 tubers), Rhabditis sp. , Mesorhabditis monhystera (17 tubers).

20

affected species 15

tubers nematode 10

of number

particular 5

The a by

0

1 2 3 4

А

14

12

affected species 10

tubers

nematode 6 8

of number particular 4 2

The a by 0

1 2 3 4 5 6 7

B

Fig. 6. Distribution of phytonematode infracommunities inhabiting potato tubers affected by Ditylenchus destructor : A — the occurrence of certain Ditylenchus destructor satellite species of phytonematodes in damaged tubers; B — the number of satellite species of phytonematodes in one damaged tuber.

As we can see, potato ditylenchosis is a complex microbiocenotic process, in which whole complexes of phytonematodes accompanying the species edificator D. destructor are involved. In affected tubers, the conditions for the existence of phytonematodes gradually create conditions for the existence of other species. Accordingly, the succession of the species composition of the nematode infracommunities occurs. At first, as a result of the vital activity of D. destructor , the healthy tissue of tubers is destroyed, subsequently it is colonized by fungi and bacteria and groups of nematodes that feed on them — mycohelminths and saprobionts. Later, conditions become unfavorable for the existence of D. destructor .

The material we analyzed clearly shows how the ratio between nematodes of various environmental groups changes in the degree of development of the disease. If at the first three stages of the disease parasitic nematodes ( Ditylenchus destructor ) comprised from 18.2 to 58.2 % of the nematode population, with the development of the disease they did not exceed 22.1–11.8 % of the nematode complex. As for mycohelminths and saprobionts, the process goes in the opposite direction. Their specific weight in the total mass of nematodes sharply increases starting from stage II and reaches a maximum at stages IV and V, when the number of mycohelminths is 51, 5, and 20.7 % of the total number of phytonematodes, respectively, and saprobionts, respectively, 26.4 and 67.4 %.

Among the mycohelminths, A. asterocaudatus (I–IV stage) and A. limbery and A.avenae (II –V stage) were more frequently recorded. A. agricola (stage III and V) and A. bicaudatus (stage II and III) were not so common. Neotylenchus sp. was found at the III-IV stage of the ditylenchosis. Among the saprobionts Ch. symmetricus (stage II–V) was usually recorded. A. buetschlii (stage II–IV), M. monhystera (stage II–IV), and D. rizophilus (stage III–V) were found quite frequently. All others were rare, they were only found in one or two stages of the process ( fig. 5 ).

I n f r a c o m m u n i t y: s p e c i e s c o m p o s i t i o n o f p h y t o n e m a t o d e s i n o n e a f f e c t e d p o t a t o, t a x o n o m i c a n d e c o t r o p h i c s t r u c t u r e o f t h e s p e c i e s c o m p l e x.

In total, 47 potato tubers affected by D. destructor were selected (fig. 6, A). The number of nematode species and their abundance in each tuber were counted (table 2). The analysis of the obtained data showed that the distribution of infracommunities by the number of species that form a complex of nematodes in one tuber is close to normal.

Only D. destructor was found in only four tubers (8.51 %). It is likely that in these cases the penetration of nematodes into the potatoes has occurred recently. All other 43 tubers were inhabited by a phytonematode complex consisting of different species (from two to seven) (fig. 6, B).

In the vast majority of cases (36 tubers, 76.6 %), the average number of nematode species (2–4) was found. In particular, in ten (21.28 %) tubers, two species of D. destructor phytohelminth nematodes and one of the mycohelminth species ( Aphelenchoides asterocaudatus or Aphelenchoides limbery ) were found in 5 cases, or 5 cases of saprobionts from five different species, three or four species of phytonematodes were recorded in one tuber 13 times, together 26 cases 53.32 %. In three species infracommunities more often there was one species of mycohelminths and saprobionts (8 cases) or, respectively, two species of mycohelminths (3 cases) or saprobionts (2 cases). Saprobionts prevailed in four species infracommunities. The ratio of 1 species of mycohelminths to 2 species of saprobionts was found 7 times. Four more times only 3 species of saprobionts were found. Mycohelminths prevailed in only two cases (2 species to 1 species of saprobionts). Probably, obtained ratios of these two ecotrophic groups of nematodes are due to the stage of the ditylenchosis.

The largest in number of species infracommunities (5–7 species) were recorded less frequently in tubers (14.89 %). In five-species infracommunities, which were recorded twice, mycohelminths and saprobionts were represented equally, 2 species of each group. Six-species groups were found three times, saprobionts prevailed in them. The ratio of mycohelminths and saprobionts, respectively, was 1 to 4, 2 to 3, and 3 to 2 species. Also in the seven-species groups that were found twice, the ratio of mycohelminths and saprobionts, respectively, was 2 to 4 and 3 to 3 species. Two species of the genus Aphelenchoides were found together only 4 times, all three species — once. Both species of Eucephalobus were recorded together also once.

The number of each of the D. destructor phytonematode satellite species varies widely, as shown above, and changes substantially during the course of ditylenchosis. In general, the average number of mycohelminths in one tuber varies from 40–45 to 320 ind., while the number of saprobionts increases from 41 to 439 ind. (table 2). So, we can assume that the relative “mass” of these two trophoecological satellite groups of D. destructor is generally comparable. At the same time, the number of the phytohelminth edificator itself varies from 10 to 540 specimens at different stages of the disease.

Figures

Fig. 3. The dynamics of the ratio of the total number of various trophoecological group nematodes during the disease of potato tubers caused by D. destructor.

Fig. 5. Occurrence of various species of phytonematodes during successive stages of the pathological process.