Biologia 67/3: 546—560, 2012 Section Zoology DOI: 10.2478/s11756-012-0025-x
Measuring the host specificity of plant-feeding mites based on field data – a case study of the Aceria species
Anna Skoracka1 &Lechos law Kuczynski´ 2
1Department of Animal Taxonomy and Ecology, Institute of Environmental Biology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61–614 Pozna´n, Poland; e-mail: [email protected] 2Department of Avian Biology, Institute of Environmental Biology, Faculty of Biology, Adam Mickiewicz University, Umul- towska 89, 61–614 Pozna´n, Poland; e-mail: [email protected]
Abstract: For the majority of eriophyoid species, host ranges have been established purely on the basis of collection records, usually without quantitative data. The aim of this study was to: (1) quantitatively examine published literature to explore whether relevant analyses of field-collected quantitative data were used to assess host specificity of herbivores; (2) propose a protocol for data analysis that could be applied to plant-feeding mites; (3) analyse host specificity of the grass-feeding Aceria species as a case study. Field data were collected in Central and Northern Europe over a period of 11 years, and included 73 grass species. For the eight Aceria species found, infestation parameters and host specificity indexes were assessed. Accumulation curves were calculated to study how the sampling effort influenced estimates of host specificity indexes. A literature analysis showed that among the studies that declared an aim of estimating the host range only 56% of them applied any quantitative analysis or informed on estimation reliability. The analysis of field-collected data and its interpretation showed the most complete and reliable conclusions about the host specificity of Aceria species when all indices were considered and, if available, other information about the mite’s ecology and biology. It was shown that estimates of host specificity could be strongly affected by sampling effort, and that several hundreds of samples should be collected for measuring the host specificity of grass-infesting mites, at least. Recommendations regarding host specificity estimation on the basis of field data are given. Key words: Eriophyoidea; host range; infestation parameters; normalized Rohde index; Rohde index; sampling effort; taxonomic index
Introduction that all host species used by a parasite are evenly in- fested. However, the hosts may differ on two funda- Host specificity is a key ecological trait of herbivore mental levels: ecological (some host species are used species as it defines their resource base, which in turn more intensely than others) and phylogenetic (some influences the population dynamics and interactions host species are closely related, whilst others are dis- of herbivores with other organisms. In addition, host tantly related). Thus, the number of host species (i.e., specificity reflects past evolutionary interactions be- host range) is in fact only a crude measure of host speci- tween the herbivore and plant lineages, thus giving ficity (Poulin 2007). A useful measure of host speci- hints about the role of historical processes in shaping ficity requires taking the level of parasite infestation ecological communities (Novotny et al. 2002). Hence, a and between-host relationships into account (Poulin & proper estimation of host specificity is one of the ma- Mouillot 2003). jor research tasks in the study of plant-herbivore inter- Estimation of the host specificity of herbivores can actions, allowing an understanding of the evolution of be based on field surveys (e.g., Gassmann et al. 2008; feeding specialization (Poulin 2007). Duyck et al. 2009). A measure of the host specificity on The term ‘host specificity’ has been used in differ- the basis of field data should take into account how ent contexts with many interpretations. According to heavily and how frequently the various host species the most widely accepted definition, host specificity is are infested by a given herbivore species. Ranking host the extent to which a parasite taxon is restricted in species according to herbivore abundance shows which the number of host species used (Poulin 2007). The hosts are used more intensively among the spectrum of term ‘host specificity’ has occasionally been used as all available hosts. Information on whether a herbivore an alternative to the term ‘host range’, however, it is utilizes its various hosts species equally or whether it useful to distinguish both terms. The number of host concentrates on only one or few of them would be valu- species infested by a parasite should be referred to as able for examination of host use (Poulin 2007). The the host range (Lymbery 1989). This measure assumes host range that indiscriminately includes all host plant
c 2012 Institute of Zoology, Slovak Academy of Sciences Host specificity of plant-feeding mites 547 records becomes rapidly dominated by marginal hosts from 1988 to November 2009 were selected by search- and accidental events (Novotny & Basset 2005). Thus, ing the SCOPUS database (http://info.scopus.com ) us- it is obvious that the assessment of the host specificity ing the following query: TITLE-ABS-KEY(”host range” basedonfieldobservationsrequires the collection of OR ”host-range” OR ”host specificity”) AND TITLE-ABS- quantitative data. KEY(”herbiv*” OR ”plant feed*” OR ”plant-feed*” OR ”phytophag*”) AND (LIMIT-TO(DOCTYPE,”ar”) OR Eriophyoid mites are an important component of LIMIT-TO(DOCTYPE,”ip”) AND (LIMIT-TO herbivore fauna in all plant assemblages and they are of (SUBJAREA,”AGRI”) OR LIMIT-TO(SUBJAREA, great practical importance as plant pests or agents in ”ENVI”). By using a more human-readable format, all pa- the biological control of weeds (Smith et al. 2010; Van pers were searched within the title, abstract or keywords Leeuwen et al. 2010). Nevertheless, most associations for: between eriophyoid mites and their plant hosts remain 1. at least one occurrence of the following terms: ”host poorly understood. Most eriophyoid species are com- range”, ”host-range”, ”host specificity”, monly regarded as highly specialized mites with narrow 2. at least one occurrence of the terms beginning with: host specificity, and only a few species are known as gen- ”herbiv”, ”plant feed”, ”plant-feed”, ”phytophag”. eralists with wide host ranges (Oldfield 1996; Skoracka Subsequently, both search criteria were combined – only papers fulfilling both of them (i.e., dealing with any et al. 2010). However, most information about the host aspects of host range or host specificity studied on plant- ranges of eriophyoid mites was based on single sam- feeding organisms) were selected. Thereafter, only research pling occasions without quantitative data. In this way, articles (either published or in press in November 2009) were the degree of host specificity of eriophyoid species could taken into account. Finally, the whole set of papers was lim- be under or overestimated due to inefficient sampling. ited to cover only the subject areas of “Agricultural and Bi- Detailed information on host plant range is scarce and ological Sciences” or “Environmental Science”. This whole limited to several species (mostly potential agents for query can be replicated by pasting it into the “Advanced the biological control of weeds) for which laboratory Search” window in the Scopus web interface. tests were applied (Smith et al. 2010). Rearing eriophy- According to the query used, 312 articles were found oid mites is very labour intensive due to their extreme on the SCOPUS database. The abstracts of all articles were screened for the aims of the study, the group of organisms minuteness and hidden life-style (Oldfield 2005), and studied and the methods used. Among the articles, 47 con- this is probably the reason for the rarity of laboratory sidered groups other than herbivores, e.g. parasitoids, plant data on eriophyoid specificity. However, field studies or animal parasites, and viruses, and were excluded from gathering quantitative data on eriophyoid mites have further analysis. Among the 265 remaining articles related also rarely been done (Skoracka et al. 2010; Smith et al. to herbivores, 208 were excluded from further analysis be- 2010). This deficiency in reliable host specificity infor- cause: (1) they did not examine host range/specificity on mation is in contrast with the diversity and importance the basis of field-collected data (they were based on molec- of eriophyoid mites, as well as with the great number of ular data – 21 articles, morphometric data – 6, experimental analogous studies targeting other herbivores (e.g., Diaz methods – 154 articles); (2) they were based on literature reviews (27 articles). et al. 2008; Duyck et al. 2009; Pratt et al. 2009) or an- From the selected 57 papers we noted: (1) the appli- imal parasites (e.g., Britton et al. 2009; Hellgren et al. cation of other methods (e.g., laboratory testing); (2) the 2009; Malenke et al. 2009). group of herbivores studied; (3) whether the aim of the study There were two main aims of this study. First, was to measure the host range or host specificity; (4) the we quantitatively examined published literature to de- application of any quantitative analysis, statistical test or termine whether quantitative field-collected data were any measures of the reliability of estimates; (5) information used by researchers to estimate the host range or host about the sample size. specificity of herbivores and what statistical analysis was applied to this data. Second, considering both the Field study value of field-collected quantitative data and the insuf- Field samples were collected between July 1998 and Octo- ficiency of such data for eriophyoid mites, we present ber 2009 from 404 localities in Central and Northern Europe results of an extensive long-term field study on grass- (Czech Republic, Denmark, Finland, Lithuania, Norway, Poland, Sweden, Ukraine). Shoots of a given grass species feeding Aceria species. It was our intention: (1) to ap- were collected by a cut just above the ground, put into plas- ply ecological parameters and indexes to obtain infor- tic bag and transported to the laboratory. Each sample con- mation on host specificity; (2) to show how sampling sisted of 10 shoots of a given grass species collected from the effort and the interpretation of various ecological in- same locality. A total of 9,420 grass shoots (942 samples) of dexes may affect our knowledge on host specificity; (3) 73 grass species were examined (Table 1). In the laboratory to show that the mere number of host species (crude mites were counted, collected from the plants by direct ex- host range) is not a reliable measure of host specificity. amination under a stereo-microscope, mounted on slides in a modified Berlese medium or a Heinze medium (Heinze 1952; de Lillo et al. 2010), and identified with a phase-contrast microscope. The generic classification followed Amrine et Material and methods al. (2003) and species classification was based on the orig- inal descriptions (Keifer 1969; Skoracka 2004; Sukhareva Analysis of the literature 1977, 1983, 1986). The taxonomic nomenclature of grass We reviewed literature dealing with the host range or host species followed the Flora Europaea Database (http://rbg- specificity of phytophagous organisms. Articles published web2.rbge.org.uk/FE/fe.html). The results presented here 548 A. Skoracka &L.Kuczynski´
Table 1. Grass species examined under study.
No. Grass species n No. AC
1 Agrostis canina L. 30 0 2 Agrostis capillaris L. 40 1 3 Agrostis gigantea Roth 30 0 4 Agrostis stolonifera L. 10 0 5 Alopecurus pratensis L. 60 0 6 Ammophila arenaria (L.) Link 40 0 7 Anthoxanthum odoratum L. 50 0 8 Apera spica-venti (L.) P. Beauv. 60 0 9 Arrhenatherum elatius (L.) P. Beauv. ex J. Presl & C. Presl. 750 1 10 Avena sativa L. 30 0 11 Avenula pubescens (Huds.) Dumort. 80 1 12 Brachypodium pinnatum (L.) P. Beauv. 30 0 13 Brachypodium sylvaticum (Huds.) P. Beauv. 40 0 14 Bromus arvensis L. 60 0 15 Bromus carinatus Hook. & Arn. 10 0 16 Bromus erectus Huds. 120 1 17 Bromus hordeaceus L. 170 1 18 Bromus inermis Leyss. 580 1 19 Bromus sterilis L. 80 0 20 Bromus tectorum L. 50 0 21 Calamagrostis arundinacea (L.) Roth 70 0 22 Calamagrostis canescens (Weber) Roth 40 0 23 Calamagrostis epigejos (L.) Roth. 470 1 24 Corynephorus canescens (L.) P. Beauv. 30 1 25 Cynosurus cristatus L. 10 0 26 Dactylis glomerata L. 540 1 27 Deschampsia cespitosa (L.) P. Beauv. 140 0 28 Deschampsia flexuosa (L.) Trin. 60 1 29 Digitaria sanguinalis (L.) Scop. 60 0 30 Echinochloa crus-galli (L.) P. Beauv. 40 0 31 Elymus caninus L. 40 0 32 Elymus farctus (Viv.) Runemark ex Melderis 10 0 33 Elymus hispidus (Opiz) Melderis 10 0 34 Elymus repens (L.) Gould 1260 1 35 Festuca altissima All. 20 0 36 Festuca arundinacea Schreb. 150 2 37 Festuca gigantea (L.) Vill. 40 0 38 Festuca ovina L. 50 0 39 Festuca pratensis Huds. 60 1 40 Festuca rubra L. 630 3 41 Glyceria fluitans (L.) R. Br. 10 0 42 Glyceria maxima (Hartm.) Holmb. 80 0 43 Holcus lanatus L. 60 0 44 Holcus mollis L. 30 0 45 Hordeum murinum L. 60 1 46 Hordeum vulgare L. 50 0 47 Leymus arenarius (L.) Hochst. 10 0 48 Lolium multiflorum Lam. 30 0 49 Lolium perenne L. 240 1 50 Lolium x hybridum Hausskn. 30 0 51 Melica nutans L. 60 0 52 Melica uniflora Retz. 40 0 53 Milium effusum L. 40 0 54 Molinia caerulea (L.) Moench 20 0 55 Phalaris arundinacea L. 200 0 56 Phleum alpinum L. 10 0 57 Phleum pratense L. 120 0 58 Phragmites australis (Cav.) Trin. ex Steud. 90 0 59 Poa annua L. 60 0 60 Poa nemoralis L. 50 0 61 Poa palustris L. 30 0 62 Poa pratensis L. 230 0 63 Poa trivialis L. 60 0 64 Puccinellia distans (L.) Parl. 60 2 65 Secale cereale L. 100 0 66 Setaria viridis (L.) P. Beauv. 20 0 67 Stipa capillata L. 20 1 68 Stipa joannis Čelak. 10 1 69 Trisetum flavescens (L.) P. Beauv. 40 1 70 xTriticosecale rimpaui Wittm. 430 1 71 Triticum aestivum L. 910 1 72 xFestulolium loliaceum (Huds.) P. Fourn. 40 1 73 Zea mays L. 140 0
Explanations: n – number of shoots examined; No. AC – number of Aceria species found. Host specificity of plant-feeding mites 549 are based on the analysis of 32,139 specimens representing than zero, it does not contribute to the sum. Thus, in this eight Aceria species. case, summation counts non-zero elements (i.e. infested host species). Data analysis Rohde index of specificity (Rohde & Rohde 2008): We calculated infestation indices for each Aceria species on each host. The following parameters were used: h P /r i=1 si si Prevalence – percentage of shoots infested: Ss = h P i=1 si k P sh ∗ sh = n 100% h where: Ss – Rohde index of specificity of species s, h –num- ber of all examined host species, Psi –meanprevalenceof where: Psh –prevalenceofAceria species s on the host h, species s on i-th host, rsi – rank of host species i (the species ksh – number of shoots of host species h infested by Ace- with the greatest prevalence has rank 1). This index takes ria species s, nh – total number of examined shoots of host into account the uneven distribution of parasites across dif- species h. This measure can be interpreted as the probabil- ferent hosts. In the numerator of this index, prevalence is ity of finding mite species s on a randomly collected shoot weighted by the inverse rank (hosts which are less used con- of grass species h. Confidence intervals for prevalence were tribute less to the sum). Thus, the value of the index is calculated using the profile likelihood method. more stable and less affected by accidental or ephemeral oc- Intensity – mean number of mite specimens per infested currences of parasite species. The higher the value of this shoot: nh index, the higher the host specificity. Maximum equals 1 1 Ish = nshi[nshi > 0] and is achieved when the parasite infests only one host. The ksh i=1 Rohde index decreases when the number of hosts increases and approaches 0 for h →∞. where: Ish – intensity of infestation of host h by Aceria Normalized Rohde index of specificity (Rohde & Rohde species s, ksh – number of shoots of host species h infested 2008): by Aceria species s, nh – number of all examined shoots of S − S S s min host species h, nshi –numberofAceria species s specimens s = 1 − Smin found on i-thshootofhostspeciesh. Brackets denote the notation of the indicator function: where: Ss – normalised Rohde index of specificity of species s, Ss – Rohde (unmodified) index of specificity of species s, 1ifx is true; [x]= Smin – minimum possible value of Ss for a given number of 0otherwise. host species h: h This means that the summation was conditional and only 1 1 Smin = covered infested shoots, i.e. those for which nshi > 0. In- h i tensity was expressed as the number of individuals per unit i=1 space (shoot) and can be interpreted as the population den- The modified index is not sensitive to the number of host sity in occupied habitat patches. Confidence intervals for species evaluated (h), therefore, it can be applied for the intensity were calculated using a bias corrected and accel- comparison of parasites using different numbers of host erated (BCa) bootstrap test (Efron & Tibshirani 1993). species. The numerical values for this index range from close Density – mean number of mite specimens per shoot: to 0 to 1. The closer to 1, the higher the degree of host speci- ficity. nh 1 Taxonomic index of specificity (Poulin & Mouillot Dsh = nshi nh 2005): i=1 h h ω P P i
the purpose of this study, we used a taxonomic classifica- tion according to the Flora Europaea Database (http://rbg- web2.rbge.org.uk/FE/fe.html). All 73 grass species which were checked for the presence of Aceria specimens were fit- ted into a taxonomic structure with four above-species hier- archical levels: genus, subtribe, tribe, and subfamily (Fig. 1). To study how the sampling effort influenced estimates of host range and host specificity indices, we constructed accumulation curves which show how the value of an index changes while the sampling progresses. However, the curve’s shape is influenced by the particular order in which samples were collected. To avoid this effect, we sampled without re- placement the entire pool of samples using different random orders. Then, the averages of 1000 of such random runs were calculated along with the 95% pointwise confidence band computed from 2.5 and 97.5 percentiles. Parameter estimates were regarded as statistically different when their 95% confidence intervals (CI) did not overlap. All computations were made in R 2.11.1 (R Develop- ment Core Team 2010). The taxonomic distinctiveness ma- trix and the phylogenetic tree were made using the ade4 package (Dray & Dufour 2007). Other packages used were: binom (Dorai-Raj 2009), boot (Davison & Hinkley 1997), lattice (Sarkar 2008), plyr (Wickham 2009), reshape (Wick- ham 2007). Some R code snippets for the calculation of host specificity indices can be downloaded from the author’s web page: http://zbiep.amu.edu.pl/lechu/R/host.spec.R
Results and discussion
Literature analysis Among the 57 (100%) studies that were related to the host range/specificity (hereafter HR) of herbivores on the basis of field-collected data the majority used only field data (81%), whereas only 19% incorporated both field and laboratory data. Laboratory tests are an es- sential step in estimating host specificity, however they results can be affected by the artificial conditions and may not correspond to the situation in natural envi- ronments (Louda et al. 2005; Pratt et al. 2009). Ideally both approaches should be combined since field studies provide a useful supplement for interpreting laboratory host range testing, and they provide a useful indication for the establishment of experimental testing (Pratt et al. 2009). The great majority of studies (97%) concerned var- ious groups of insects, whereas only one paper consid- ered mites, one paper studied nematodes, and one pa- per studied amphipods. This was not a surprise since insects represent more than half of all known living or- ganisms, and the most diverse groups within the in- sects appear to have coevolved with flowering plants (Chapman 2009; Wilson 1992). Little attention given to host specificity of herbivorous mites is however surpris- ing given the economical importance of plant-associated mites, both as agricultural pests and biocontrol agents. In 32 papers (56%) the aim of the study was de- clared as host range (HR) estimation. From these how- ever, only 18 papers (56%) contained some quantitative analysis or included information on estimation reliabil- ity (sample size or error measures). From 25 papers Fig. 1. Taxonomy of grass species collected and used in this study. which did not declare the aim to be HR estimation, 21 Host specificity of plant-feeding mites 551
Table 2. Summary of host specificity indices, population density and the interpretation of host specificity of Aceria species.
Crude Normalized Host range host Rohde Rohde Taxonomic after Aceria species range index index index Population density interpretation Host specificity
A. aculiformia 3 0.77 0.41 2.9 high on 1 host, 2 at least two moderate on 2nd host taxonomically distinct hosts A. calamagrostis 1 1 1 – extremely low 0 no grass host A. erecti 2 0.96 0.83 4 high on 1 host 1 specialist: one reliable host A. eximia 2 0.96 0.83 3 high on 1 host 1 specialist: one reliable host A. flexuosae 1 1 1 – moderate 1 specialist: one host A. glomerivagrans 2 0.76 0.15 3 similar on two hosts 1 one reliable host A. stipaespinulata 2 0.99 0.97 1 high on two hosts 2 two congeneric hosts A. tosichella 14 0.42 0.24 3.6 various on different hosts 10 generalist papers contained sufficient information for an estima- ble behaviour of the mean (Fig. 2B). The value of the tion of HR and reported measures of estimation relia- modified Rohde’s index was even more stable and did bility. Altogether, from the total of 57 papers related not change substantially while sampling. The asymp- to HR estimation from field data, 39 (68%) contained totic value of this index was 0.412 (CI: 0.403–0.426). quantitative results and some figures of estimation er- However, the changes in the confidence band were sim- ror. Thus, despite its theoretical and practical impor- ilar to those of the unmodified version of this index tance, field-based research on the host specificity of her- and became narrower at the sample size of about 500 bivores still has many methodical gaps and thus may (Fig. 2C). lead to unreliable conclusions. None of the 57 studies re- The taxonomic host specificity index increased latedtoHRofherbivoresonthe basis of field-collected while as the sampling advanced and finally reached the data used Rhode indexes or taxonomic index. value of 2.950 (CI: 2.948–2.953); its confidence band abruptly narrowed when the sample size exceeded 500 Host specificity of Aceria species (Fig. 2D). The value of this index was almost maxi- Eight Aceria species: Aceria aculiformia Sukhareva, mal, suggesting a high taxonomic distinctness among 1986, A. calamagrostis Sukhareva, 1977, A. erecti Sko- the host species. Indeed, grasses hosting A. aculiformia racka, 2004, A. eximia Sukhareva, 1983, A. flexuo- belonged to three different genera, and one them be- sae Skoracka, 2004, A. glomerivagrans Skoracka, 2004, longed to a different subtribe (Fig. 1). A. stipaespinulata Skoracka, 2004, and A. tosichella The values of both Rohde’s indices and the taxo- Keifer, 1969 were found on 23 (31.5%) grass species nomic index indicate that A. aculiformia is not highly out of the 73 examined. These mite species differed in specialized towards only one host species. Indeed, this their host ranges, host specificity indices and infesta- mite was recorded on three grass species, however, the tion parameter values. The most complete and reliable parameters of infestation varied among the infested interpretation of the host specificity can be drawn when hosts. The most heavily and frequently infested was all indices and parameters are considered, and, if avail- Puccinellia distans – the prevalence on this host was able, other information about the ecology and biology 58.3% (CI: 45.7%–70.3%), the infestation intensity was of mites. Such interpretation is presented below and in 67.7 (CI: 33.8–128.6) and population density was 39.5 the Table 2. (CI: 19.1–79.1). The probability of finding A. aculi- formia on Festuca rubra was 43.8% (CI: 40.0–47.7); Aceria aculiformia however, the intensity of infestation (20.1; CI: 16.6– A great sampling effort was needed for reliable estima- 25.4) and population density (8.8; CI: 7.1–11.2) were tion of the values of three indices of host specificity much lower than on P. distans. Lolium perenne was (both Rohde’s indices and the taxonomic index) for sparsely infested. In spite of a great number of shoots A. aculiformia. Reliable estimation of these indices was inspected (Table 2) the probability of finding A. aculi- achieved when the number of samples exceeds several formia on this grass species was only 3.3% (CI: 1.5%– hundred (ca. 500 in this case). 6.1%). The infestation intensity (6.0; CI: 3.1–8.8) and The asymptotic value of the Rohde’s index was population density (0.2; CI: 0.1–0.4) were both ex- 0.771 (CI: 0.767–0.778). The value of this index de- tremely low on L. perenne, what indicates that this creased when the number of collected samples increased host species is infested incidentally. The mites might and finally reached an asymptote at about 700 samples. have encountered this grass species by accident dur- At the lower number of collected samples the value ing their dispersal by wind or phoresy (Michalska et al. of the index was high (almost maximal), which may 2010). Thus, we suggest that L. perenne should not be suggest that A. aculiformia is highly specific. However, included in the host range of A. aculiformia.Moreover, the confidence band was wide and thus the index had the host species accumulation curve (Fig. 2A) was rel- a limited diagnostic value at low numbers of samples. atively steep and reached the asymptote at about 800 The confidence band became narrower when the sam- samples. It showed that it is relatively easy to detect ple size approached 500, corresponding to a more sta- two host species for A. aculiformia. Thus, we can confi- 552 A. Skoracka &L.Kuczynski´
Fig. 2. Accumulation curves with 95% confidence bands computed for host range and specificity indices for Aceria aculiformia. dently conclude that P. distans and F. rubra can be in- Aceria erecti cluded within the host range of A. aculiformia, however Two plant species were recorded as hosts for this mite the latter as the host on which the mite has less success species, although their infestation varied substantially. than on the former. This may result from the various The population density on Bromus erectus was sig- conditions that the mite meets on the hosts, e.g. plant nificantly higher (13.9; CI: 10.7–17.7) than on Fes- quality, plant defence, and the presence of predators, tuca arundinacea (0.9; CI: 0.3–2.3). The probability which prevent the mite from developing large popula- of finding A. erecti on B. erectus was almost 51.0% tions (Jaenike 1990). However, the role of these plant (CI: 41.9%–59.7%), whereas on F. arundinacea it was species in the host specificity pattern of A. aculiformia only 4.7% (CI: 2.0%–8.8%). The infestation intensity, can only be explained experimentally. although higher on B. erectus (27.4; CI: 22.8–33.2), did not differ significantly from that on F. arundinacea Aceria calamagrostis (18.9; CI: 7.6–35.7). The taxonomic host specificity in- This mite species was found on only one host (Fes- dex was constant and its value was 4, which reflected tuca rubra) with very low infestation intensity (2.5; CI: the highest taxonomic distinctness between these two 1.0–2.5) and population density (0.01; CI: 0–0.03). The host species (Fig. 3D). Both hosts belonged to different probability of finding this mites species on F. rubra was tribes (Fig. 1). only 0.3% (CI: 0.05%–0.1%). Both Rohde indices hit The host species accumulation curve for this mite their maximal values in this case (Table 2) what sug- species did not reach an asymptote (Fig. 3A). This gest that A. calamagrostis is a strict specialist on F. means that our knowledge on the hosts inhabited by rubra. However, the extremely low values of mite in- A. erecti is incomplete and discoveries of further host festation may indicate that the mite is not successful species should be expected. on F. rubra and that its occurrence here was acciden- The Rohde’s index accumulation curve exhibited a tal. This species was originally described from Calama- slight decrease with increasing sample size and reached grostis arundinacea L., in Russia (Sukhareva 1977). Un- the value of 0.958 (CI: 0.954–0.966). This high value fortunately, information about the parameters of mite indicates that of the two host species, A. erecti was pre- infestation in Russia was not available. Among the 70 dominantly concentrated on one of them. At the lower shoots of C. arundinacea and 510 shoots of other Cala- number of samples the value of this index was near 1 magrostis species inspected during this study A. cala- and the confidence band was relatively narrow, suggest- magrostis was not found on any of them. Thus, the ing easy detection of one of the two known host species host specificity of A. calamagrostis cannot be estimated (Fig. 3B). Then the estimation uncertainty increased without more ecological or experimental data. On the (the accidental species was more likely to be found when basis of the data collected up until now, F. rubra cannot sample size grew, causing a rise in variation) and then be included within the host range of A. calamagrostis. decreased again for larger samples (the estimation be- Host specificity of plant-feeding mites 553
Fig. 3. Accumulation curves with 95% confidence bands computed for host range and specificity indices for Aceria erecti. came more reliable due to increasing sample size). The intensity (42.3; CI: 33.9–53.8), population density (9.1; modified Rohde’s index accumulation curve increased CI: 6.8–12.1) and prevalence (21.5%; CI: 17.9%–25.3%) with increasing sample size and reached the highest were significantly higher on Calamagrostis epigejos value of 0.829 (CI: 0.815–0.841). The reliability of es- than on Festuca rubra (infestation intensity: 2.8; CI: timation as indicated by the confidence band increased 2.0–3.5; population density: 0.02; CI: 0.003–0.04; preva- with the sample size (Fig. 3C). lence: 0.6%; CI: 0.1%–1.4%). The taxonomic host speci- Because B. erectus was the host plant infested most ficity index was constant and equalled 3 (as both hosts heavily and frequently by A. erecti a moderate sam- belonged to different subtribes) (Fig. 4D). pling effort was needed to detect this plant species in The accumulation curves for A. eximia (Fig. 4) the host range of this mite. To detect F. arundinacea were almost identical to those computed for A. erecti in the host range of A. erecti a higher sampling effort (Fig. 3) and could be interpreted in a similar way, i.e. was required, what may suggest that this is not a pre- that knowledge about the host range of A. eximia is ferred host plant for this mite. However, when the mite incomplete. The values of the Rohde’s indices suggest occurred on F. arundinacea it infested the plant very that A. eximia prefers a single host species. Aceria ex- intensely and reached a high abundance. The values imia was described as a mite associated with C. epige- of the both Rohde’s indices also suggest that A. erecti jos in Russia (Sukhareva 1983), and no other hosts have prefers a single host species. Wide confidence intervals been recorded for this mite species. Thus, at the present (Cl) around the mean of infestation intensity of F. arun- state of knowledge, only C. epigejos can be considered dinacea, and the peculiar shape of the CI around the as a certain host for A. eximia,andF. rubra as an ac- accumulation curves of both Rohde’s indices indicate cidental host (Table 2). some abnormality in the phenomenon of F. arundinacea infestation by A. erecti. The infestation behaviour of A. Aceria flexuosae erecti towards F. arundinacea is the reason why the host Only one host species, Deschampsia flexuosa was de- range accumulation curve did not reach an asymptote. tected in the host range of Aceria flexuosae.Theval- Thus, at the present state of knowledge, B. erectus can ues of infestation were moderate: intensity was 5.2 be considered as a confirmed host for A. erecti,whereas (CI: 3.5–7.1), population density was 0.7 (CI: 0.3– the role of F. arundinacea in the host specificity of this 1.4), and prevalence was 13% (CI: 6%–23%). Thus, mite is uncertain (Table 2). one could suspect that D. flexuosa is not the favoured host for A. flexuosae. However, earlier observations Aceria eximia showed that populations of A. flexuosae found on D. Two grass species with different values of infestation flexuosa consisted of all stages, including juveniles and were recorded as hosts for A. eximia. The infestation eggs (Skoracka 2004), which suggests that this host 554 A. Skoracka &L.Kuczynski´
Fig. 4. Accumulation curves with 95% confidence bands computed for host range and specificity indices for Aceria eximia. is accepted by the mite for oviposition and develop- Despite no significant differences in the parameters ment. of infestation between the two plant species recorded for The values of the Rohde index and the modified A. glomerivagrans,onlyD. glomerata can be considered Rohde index were 1. In the present state of knowledge as a confirmed host (Table 2). Information on xF. loli- this mite species can be considered as a strict specialist, aceum is not reliable due to the small sample size which which occasionally occurs (Table 2). resulted in wide confidence bands around the means of all three parameters and unstable values of Rhode’s in- Aceria glomerivagrans dices. Thus, at this time we had insufficient informa- The mite was collected from two host species. Although tion to determine the role of xF. loliaceum in the host there were no significant differences in the parameters range of A. glomerivagrans. In this case, apart from ex- of infestation, this mite reached a higher infestation in- perimental testing, increasing the sampling effort could tensity (10.1; CI: 8.3–12.5) and population density (1.3; bring better results. CI: 1.0–1.8) on Dactylis glomerata compared to xFes- tulolium loliaceum (7.0; CI: 3.8–9.5 and 0.7; CI: 0.2– Aceria stipaespinulata 1.8, respectively). The probability of finding this mites This mite was recorded on two host species, Stipa joan- species on D. glomerata was 13.3% (CI: 11.0%–16.4%), nis and S. capillata and values of all infestation pa- whereas on F. loliaceum it was 10.0% (CI: 3.2%–21.7%). rameters were not significantly different on both plant The taxonomic host specificity index was constant. The species. The prevalence on both host species was similar value of 3 indicates taxonomic distinctness between the and quite high (90.0%). On S. joannis population den- two host species at the level of subtribes (Figs 1, 5D). sity was 19.3 (CI: 12.0–31.7) and infestation intensity The host species accumulation curve for A. glom- was 21.4 (CI: 14.2–34.3), whereas on S. capillata the erivagrans did not reach an asymptote (Fig. 5A), sug- values were 10.6 (CI: 7.6–13) and 11.7 (CI: 8.9–14.6), gesting that our knowledge on the host range of this respectively. The taxonomic host specificity index was species is incomplete. constant and equalled 1 (Fig. 6D) (both hosts belonged The Rohde’s index accumulation curve decreased to the same genus, Fig. 1). and did not reach an asymptote either. Its final value The Rohde’s index accumulation curve decreased was 0.791 (CI: 0.768–0.907). The confidence band was and then increased again up to the value of 0.993 (CI: very wide throughout the sampling, indicating that re- 0.885–1.000), but did not reach an asymptote. This be- liable estimation was not possible (Fig. 5B). The mod- haviour is difficult to interpret and the wide confidence ified Rohde’s index accumulation curve (final value: band implies that the estimation of this index was not 0.154, CI: 0.072–0.340) showed unstable and unpre- very reliable (Fig. 6B). The modified Rohde’s index ac- dictable behaviour and could not be used for drawing cumulation curve exhibited an almost linear increase any serious conclusions (Fig. 5C). with increasing sample size and finally reached the Host specificity of plant-feeding mites 555
Fig. 5. Accumulation curves with 95% confidence bands computed for host range and specificity indices for Aceria glomerivagrans.
Fig. 6. Accumulation curves with 95% confidence bands computed for host range and specificity indices for Aceria stipaespinulata. value of 0.970 (CI: 0.538–1.000) with a very wide confi- that our knowledge about the host richness for A. sti- dence band throughout all values of simulated sampling paespinulata is far from complete (Fig. 6A). We can ex- (Fig. 6C). pect that other Stipa species belong to the host range The host range accumulation curve did not reach of A. stipaespinulata, thus additional sampling is rec- an asymptote with increasing sample size which means ommended. 556 A. Skoracka &L.Kuczynski´
Fig. 7. Infestation parameters of Aceria tosichella.
At the present stage of knowledge, we can conclude distinctness existed between all host species occupied that this mite species has two congeneric hosts, and that by A. tosichella (Fig. 8D). The host plants infested by it is therefore a genus specialist (Table 2). this species belonged to different genera, subtribes, and tribes (Fig. 1). Aceria tosichella The Rohde’s index accumulation curve exhibited Fourteen plant species were recorded as hosts for this a decrease and reached the value of 0.415 (CI: 0.400– mite species. The parameters of infestation differed 0.439). However, it did not reach a definite asymptote. greatly among the hosts, and some of them were charac- The confidence intervals were quite narrow, which en- terized by untypical parameters of infestation. Triticum abled accurate and reliable estimation (Fig. 8B). The aestivum and Festuca arundinacea clearly stood out modified Rohde’s index accumulation curve slightly de- from other hosts by achieving the highest values of creased with increasing sample size and reached the intensity (35.2; CI: 5.9–106.2 and 36.0; CI: 24.3–48.5, asymptotic value of 0.237 (CI: 0.218–0.266) (Fig. 8C). respectively) and, simultaneously, very low prevalence To sum up, several grass species of varying taxo- values (2.7%; CI: 1.8%–3.9% and 5.3%; CI: 2.5%–9.7%, nomic relatedness were noted as hosts for A. tosichella. respectively). This means that A. tosichella infested All indexes indicated a low host specificity of this mite these hosts very rarely but with a great potential to species. Moreover, the host range accumulation curve rapidly increase population numbers. This is the oppo- did not reach an asymptote with increasing sample size site situation to the following grasses: Hordeum mur- which means that our knowledge on the host richness inum, Elymus repens, Corynephorus canescens, Trise- for A. tosichella is still incomplete (Fig 8A), and the tum flavescens onwhichthemitegainedhighormod- host range of this mite may increase during subsequent erate prevalence, but a low intensity of infestation. This sampling. Thus, A. tosichella seems to be a generalist means that the probability of finding A. tosichella on species (Table 2), which is unusual for eriophyoid mites these hosts was high, but the populations were not (Skoracka et al. 2010). very dense. This phenomenon was particularly observed Different strategies displayed by A. tosichella when with H. murinum, which was the most frequently in- infesting different host plants may result from various habited host by A. tosichella (prevalence 53.3%; CI: conditions created by a specific host. Such conditions 40.7%–65.6%), but with a moderate population den- have a great influence on the host acceptance decision sity on the occupied habitat patches (infestation inten- and the life history traits of herbivore species (Jaenike sity 15.5; CI: 10.1–22.3). Four other hosts, i.e., Avenula 1990; Agrawal et al. 2002; Chapman 2003), which fur- pubescens, Festuca pratensis, Arrhenatherum elatius, ther induce species presence and abundance on the and Bromus inermis, were characterized by moderate plant. If A. tosichella is a fully generalist species, then values of prevalence and infestation intensity. A few after encountering any hosts belonging to its host range hosts had very low parameters of infestation, thus they this mite is able to easily acclimate to the host condi- were probably accidentally found in the host range of A. tions; however, its life history traits may differ on dif- tosichella. This concerns Puccinellia distans, Bromus ferent hosts. Such an effect has been previously demon- hordaceus, Agrostis capillaris, and especially xTriti- strated for other herbivores (e.g., Awmack & Leather cosecale rimpaui, for which a great sampling effort was 2002; Raghu et al. 2004). Another possibility is that made (Fig. 7, Table 1). differences in host infestation are a result of different The accumulation curve of the taxonomic host dispersal capacities and intrinsic population character- specificity index reached the asymptote at a few hun- istics of specialized host populations of the mite, which dreds of collected samples. The final value was 3.555 evolved as an adaptation to the specific host plant (Ma- (CI: 3.548–3.564), which meant that a high taxonomic galh˜aes et al. 2007). In this case, A. tosichella repre- Host specificity of plant-feeding mites 557
Fig. 8. Accumulation curves with 95% confidence bands computed for host range and specificity indices for Aceria tosichella. sents a complex of specialized host races or even cryptic Conclusions species. This concept is very likely since there are some indications that A. tosichella may represent a species Despite its great importance, research on the host speci- complex (Carew et al. 2009). ficity of eriophyoid and other herbivorous mites has pro- In spite of the huge sampling effort in the case of gressed slowly. Detailed information on the host plant wheat, T. aestivum, a wide confidence band can be seen range is only available for a minority of species (mostly around the mean value of intensity. This is the result potential agents of biological weed control), for which of an uneven distribution of the mite on the host spec- host specificity tests were applied. For the majority of imens. The range of the number of mites per infested species the host ranges were established on the basis of tiller was 1–450. Bearing in mind the above interpreta- new collection records; unfortunately these were usually tion of infestation parameters, it can be confirmed that without quantitative data (Skoracka et al. 2010; Smith A. tosichella hardly ever attacks wheat, but when it et al. 2010). However, information on the abundance does, it becomes aggregated on a few plants and builds of a herbivore on a particular plant species relative to dense populations. This result is opposite compared to other plant species is principal to understanding the the role of A. tosichella infesting grasses in other re- role of each plant species in herbivore ecology (Walter gions in the world, such as North and South America, & Benfield 1994). Australia, many Western European countries, Asia, the Reliable knowledge on host specificity is especially Middle East, Africa, and Oceania. In most of these ar- important in respect to species which are of econom- eas A. tosichella was recorded almost exclusively on ical importance as direct pests or as vectors of plant wheat, and was responsible for huge losses in wheat viruses. Alternative hosts for the herbivore may be cru- production, mostly due to its ability to transmit plant cial in the epidemiology of the vectored viruses and for viruses (Navia et al. 2010). Other wild or cultivated maintaining the population of herbivores when agricul- grasses were considered as alternative hosts by this mite tural hosts are not readily available (Norris & Kogan species (Harvey et al. 2001). It would be interesting 2005). Information on true host ranges may be useful to find out whether this mite attacks wheat in other for understanding the ability of a herbivore to colonize areas in the world in a similar way, i.e. sporadically, alien plants as well as native plants of economical signif- but with a great infestation intensity. Such information icance, and thus for predicting the ability of herbivore could explain the infestation behaviour related to the species to become invasive in new areas (Navia et al. losses this mite causes. Unfortunately, no parameters 2010). describing the infestation of wheat and other grasses in Host specificity as a quantitative unit has received other areas of the world were available in the literature, additional interest within the last few decades as a therefore no comparisons are possible. promising predictor of local as well as global patterns 558 A. Skoracka &L.Kuczynski´ of biodiversity. A great number of such analyses, using and used for interpretation as they give another insight herbivorous insects as the model group, have been pro- into the data. vided (e.g., Ødegaard et al. 2000; Novotny et al. 2002; 6. When reporting any parameters based on any Novotny and Basset 2005; Dyer et al. 2007). Due to the sampling protocol (including infestation parameters lack of basic knowledge on the host ranges of most phy- such as prevalence, density or intensity), error measures tophagous mites, especially eriophyoid mites, such in- must always be given. As distributions of these param- vestigations are impossible with this taxon. Filling this eters are usually skewed or truncated (density, inten- gap would be advantageous for studying beta diversity sity) and are often very close to their extreme possible since herbivorous mites are a significant component of values (prevalence), we strongly discourage the use of plant-associated fauna. parametric approximation methods. The testing of host specificity can never entirely 7. Employing standardized analyses for a broad be truthful until all possible plant species for the whole scale of field studies and species would allow the mea- range of herbivore species are included (i.e., one can surement of herbivore host specificity on a larger scale, never prove monophagy). Consequently, host specificity not just locally, and thus the investigation of problems is a relative measure dependent on both temporal and concerning the ecology and evolution of the whole herbi- spatial scales. In this study, field data were gathered vore group. A standardized protocol would also permit from many areas in Central and Northern Europe over comparisons of the infestation of injurious and invasive more than 11 years and thus take into account the species in various regions throughout the world. This spatial and seasonal variations in mite diversity and would facilitate monitoring of these species. abundance. However, to make the results more accu- 8. Finally, we should be aware that the phe- rate these observations should be expanded in more ar- nomenon of host specificity is unusually complex. The eas and should include more plant species. judgment about host specificity is not straightforward It may seem that the information and recommen- and further information on the biology and ecology of dations given in this article are well-known and obvi- studied organisms will surely change the state of our ous. However, due to the deficiency of studies based on knowledge. field-collected data which enable a reliable estimation of the host specificity of eriophyoid mites we decided to outline these issues in a bit more detail. Our recom- Acknowledgements mendations regarding host specificity estimation based We thank the reviewer for helpful remarks on the manu- on field data are summarized below. script. The study was supported by the Polish Ministry of 1. 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