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Article

Assessing the Importance of Natural Regulating Mechanisms in Weed Management: The Case of Weed Seed Predation in a Winter Wheat Field and in Adjacent Semi-Natural Habitat in Northern Hungary

1
Department of Integrated Plant Protection, Plant Protection Institute, The Hungarian University of Agriculture and Life Sciences (MATE), 2100 Godollo, Hungary
2
Weed Research Department, Integrated Agricultural Pests Management Research Centre, Agricultural Research Corporation (ARC), Wad Madani P.O. Box 126, Sudan
3
Bayer Hungaria, 1117 Budapest, Hungary
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(11), 2666; https://doi.org/10.3390/agronomy12112666
Submission received: 10 September 2022 / Revised: 22 October 2022 / Accepted: 24 October 2022 / Published: 28 October 2022

Abstract

:
Weeds are one group of pests that significantly reduce crop yields and qualities, while herbicide use poses a risk to human health and environment. Weed seed predation has been identified as a potential biocontrol approach offering sustainable weed management. It causes substantial seed losses on weed species in crop fields, and thus may result in a reduction in herbicide use. This study aimed to investigate the relevant seed predation patterns on important weed species, Galium aparine L., Papaver rhoeas L., and Apera spica-venti L., in a winter wheat field and the adjacent semi-natural habitat (SNH) near Gödöllő, Hungary, assuming that weed seeds are likely to be predated, but predation levels may differ by weed species and habitat type. Sampling rounds were performed twice, in 2019 and 2021, before crop harvest, by placing a total of 240 seed cards (120 cards/round) on the soil surface inside both crop field, and in the adjacent SNH. Seed predation was assessed on each card every 24 h, for 5 days in 2019 and 6 days in 2021. The results revealed high intensity (100%) of seed predation on the evaluated weed species, during the exposure periods in both years and habitat types, although weed seeds were significantly consumed (p < 0.001) in 2019 as opposed to 2021. Whereas, seed consumption levels were not significantly different (p = 0.802) among habitat types, and between habitats and years (p = 0.842). The optimum period for measuring weed seed predation was found to be after 48 h of field exposure. Our findings showed that seed predation reduced the number of exposed weed seeds on the soil surface, which may decrease the weed seed banks, and the number of weed seedlings the next cropping season.

1. Introduction

Weeds are one group of pests (“Any species, strain or biotype of plant, animal or pathogenic agent injurious to plants or plant products” [1], revised [2,3], revised [4]) that compete with field crops and thus reduce their yields and quality [5]. Weed control and management has been based on a wide range of tools (mechanical, physical, agronomic, and biological), predominantly on chemical herbicides. For instance, herbicides account for more than 40% of the overall consumption of an average of 179,798 tons/year of pesticides in the European Union (EU) [6], which has pushed many governments to apply strict restrictions on herbicides utilization [7]. The need for identification of sustainable weed management alternatives was raised a decade ago [8]. In the EU, the reduction of the risk of synthetic pesticides to human health and environment is phrased under the Integrated Pest Management (IPM) approach in the Framework Directive on the Sustainable Use of Pesticides [9] (Directive 2009/128/EC). In line with this approach, Integrated Weed Management (IWM) has become better known and followed in recent years. Its implementation creates a balance of weed control (e.g., reducing their impacts on crops yield and the potential for weed resistance), while preserving the botanical diversity of weed species and weed seed predators. Consequently, conservative biological weed control has become a focus for many researchers.
There is a need to place the crop–weed relation into a spatial context, e.g., in the crop field and non-crop habitats (field margins and adjacent semi-natural habitats SNHs) on a farm and landscape level. The presence of SNHs around crop fields is crucial for biological weed control, as they host many beneficial organisms [10,11,12,13], and many of them are potential weed seed predators [14,15]. Furthermore, SNHs provide natural enemies with food, shelter, and hibernating habitats. Therefore, good landscape management is expected to improve the role of SNHs, thus strengthening biocontrol functions in agricultural landscapes [16]. Additionally, SNHs are important in sustaining insect natural enemies that move from SNHs into adjacent fields after winter or later in the season [17].
The adoption of management strategies that support the delivery of ecosystem services in crop fields has become an essential concern for increasing agricultural production [18]. The ecosystem service of weed seed predation by natural weed seed predators has been shown as an effective ecological service for weed management in crop fields [19]. It results in decreasing the frequency of weed species in agroecosystems, the spread of invasive species in SNHs [20,21], and suppression of weed population densities [22,23,24], since weed seeds are considered a major food for many animals, including vertebrates and invertebrates [25,26]. Some carabid species were found to efficiently consume weed seeds under laboratory conditions [27], whereas other species showed responses to weed seed patches in the fields [28,29]. Such feeding behaviour on the fresh weed seeds (also called post-dispersal weed seed predation) is considered as a regulatory ecosystem service for weed management.
Seed predation occurs in two forms at different times: pre-dispersal predation, which occurs while the seed is still on the crop and is not yet ripe, and post-dispersal seed predation, which occurs on or in the soil surface or on another substrate after seed shedding, when the seeds are exposed to consumption by seed predators. Various studies have indicated the dominance of invertebrate seed predators in agricultural systems [28,30,31] and their contribution is reported to be approximately 80 to 90% of the total seed predation [15]. Weed seed losses caused by weed seed predators have been reported to be substantial in many cases [32]; however, they do vary over years [33,34] and across fields [35,36,37]. Recent results in Hungary showed seeds of different weed species have been similarly consumed in maize fields, but seed consumption levels differed significantly between years [38]. Nevertheless, weed seed predators have been observed to reduce weed seed density by 50% on average [39], which can contribute to reducing weed population growth. For example, Westerman et al. [23] reported that the percentage of cumulative seed predation can lower the population density of the weed species Abutilon theophrasti while higher carabid seed predators’ abundance has been positively associated with weed seedbank changes throughout the cropping season, suggesting that seed predator behaviours can govern weed seedbanks [8]. As a result, weed seed predation can be employed for weed management, helping to reduce the current reliance on herbicides [40]. However, the substantial variability in weed seed predation rates between studies has been an obstacle to the adoption of weed seed predation in weed management programs [41,42,43].
Seed predation causes significant weed seed losses in agricultural fields and can, therefore, contribute to weed management [44], but many factors may affect its effectiveness. For example, SNHs adjacent to the crop fields have been found to be advantageous for crop protection and sustainability [45]. These habitats are particularly favourable for beneficial invertebrate species seeking to overwinter, as they are less disturbed; this also allows such species to easily obtain access to the fields later [46,47]. In addition, SNHs are important standard habitats for seed predators and thus a population source for field colonisation [48,49]. In Hungary, Kiss et al. [46,49] confirmed the presence of invertebrate seed predator individuals, mainly Carabidae, inside winter wheat fields and in the field margins. Another evident example shows the peak of mixed feeder individuals of Harpalus and Amara species surveyed in a winter wheat field and in its borders in Kartal, Northern Hungary, in June–July 1994. [46]
Winter wheat (Triticum aestivum L.) is the second most commonly cultivated crop in Hungary, [50] grown on about a million hectares. According to the sixth National Arable Field Weed Survey (2018–2019) in Hungary, the most important weed species of winter wheat fields were Stellaria media L., Ambrosia artemisiifolia L., Apera spica-venti L., Papaver rhoeas L, Galium aparine L., and Chenopodium album L. The Department of Integrated Plant Protection of MATE (former SZIU) University carried out the first surveys in winter wheat fields in Hungary within the QUESSA (Quantification of Ecological Services for Sustainable Agriculture) EU project (2013 to 2017), which has become the ground for subsequent research work in this field.
The present study was based on participation of invertebrates as seed predators, specifically, activity density, key mixed feeder species, and their phenology from previous studies by Kiss et al. [49], in a winter wheat field and in the adjacent SNHs, in Kartal, Northern Hungary, near our study area. They confirmed the occurrence of arthropods invertebrate seed predator individuals, mainly Carabid individuals such as Harpalus and Amara species. This provides evidence for the potential role of ground-dwelling arthropods as seed predators. The objective of this study was to assess seed predation patterns on three important weed species, G. aparine, P. rhoeas, and A. spica-venti, inside a winter wheat field and the adjacent SNH in 2019 and 2021, near Gödöllő, Northern Hungary. We hypothesized that weed seeds are likely to be predated by seed predators, but predation levels may differ by weed species and habitat type.

2. Materials and Methods

2.1. Study Site and Experimental Setup

Field experiments of invertebrate weed seed predation were performed in a winter wheat field and the adjacent SNH at the Hungarian University of Agriculture and Life Science (MATE) research farm (Szárítópuszta) (47.5803° N, 19.4014° E) near Gödöllő, Hungary. The crop rotation in the study area usually includes winter wheat, barley, oil seed rape, pea, sunflower, and maize. The field edge is undisturbed and consisted of small forest patches and herbaceous undergrowth with grasses. The soil type is rust-brown forest soil (Chromic Luvisol). The climate is continental, with frequent weather extremes. The mean annual temperature is 9.7 °C, and the average annual precipitation is 550 mm, two-thirds of which falls between April and September.

2.2. Assessment of Seed Predation

During this investigation, 20 fresh seeds of each weed species G. aparine L., P. rhoeas L., and A. spica-venti L., ordered from Herbiseed® (Twyford, Reading, UK), were glued (glue spray adhesive: 3 ML, 400 mL/282 g), to sandpaper cards’ surfaces (25/10 cm, p = 60 (kL361 J-Flex Klingspor, Hickory, NC, USA) (Figure 1). The p = 60 roughness was chosen to closely resemble the soil surface of the experimental site in both colour and roughness, while the adhesive strength ensured that the seeds would not be displaced under normal weather conditions (wind and rainfall) or during the placement of the cards. An exclosure treatment featuring wire mesh (hole size 25 mm) was used to allow easy access of small invertebrates while preventing entry to and securing the seed cards against the larger vertebrate predators (Figure 2).
Two sampling rounds were performed in a winter wheat field and in the adjacent SNH in June of 2019 and 2021, prior to crop harvest and after the seed ripening of the assessed weed species. The sampled SNH was deemed to be that habitat which is wider than one meter and adjacent to the winter wheat field (small forest patch). The experiment was designed as follows: a total of 240 seed cards (120 cards per round or year) were placed horizontally on the soil surface (Figure 2), with 60 seed cards placed inside the wheat field at a distance of 10 m from the field edge, and another 60 seed cards were fixed inside the adjacent SNH. The 60 seed cards were arranged along 20 transects, with 3 cards per transect (1 card for each weed species), distanced by 10 m between transects, and 1 m between cards. Due to unfavourable meteorological conditions (continuous rain fall) in the last days of field exposure, the exposure lengths differed, lasting for 5 days in 2019 and 6 days in 2021. The number of seeds remaining on each card was recorded every 24 h, beginning 24 h after the first day of field exposure. Small-size weed seeds, e.g., P. rhoeas were counted by using a manual magnifier. The number of seeds remaining on the cards was thereby converted into a proportion representing seed predation relative to the total number of glued-on seeds.
The winter wheat field was visually checked during the above period to assess the presence or holes of potential weed seed consumers such as (Microtus arvalis and other small mammals). Additionally, the seed cards were carefully checked to detect footprints or excrements of potential seed feeder birds.
Identifying and choosing the optimum exposure period and time for estimating weed seed predation levels was challenging. Most of the relevant previous studies assessed seed predation during long-term exposure periods, ranging from a couple of weeks to several months [51,52,53]. In our study, however, to achieve accurate estimates of seed predation levels, data on seed predation from day 0 to day 2 (48 h exposure period) were used, based on the low number of remaining seeds left on the final days of the field exposure. This supported the finding that a suitable exposure time for estimating weed seed predation in winter fields could be 2 days (48 h) after first field exposure.
Data collection included the number of seeds removed and the seeds remaining on the cards after 5 and 6 days of exposure in the field. The counting of the remaining seeds on each card may thus have been influenced by human errors during the counting process. Statistical data analyses were performed using R statistical software (version: 4.1.1, R Development Core Team 2021), including the application of linear models and single-factor analysis of variance (ANOVA). Binomial models were also fitted and validated at seed and card levels to compare seed predation between weed species and years. Diagnostic plots of residuals were investigated to ensure model fit assumptions [54].

3. Results

Seeds of all seed cards placed either inside the winter wheat field or at the adjacent SNH were consumed to a certain percentage in both years. There was a high intensity of seed predation in most cases: 100% consumption was observed in 70–100% and 30–58% of cards during the exposure periods of 2019 and 2021, respectively (Table 1). The number of the remaining seeds on the cards monotonically decreased from the first day of exposure in both years, and more than 75% of the seeds were consumed after 3 days of exposure (Table 2).
Furthermore, there were significant differences on seed predation levels between the two study years (p < 0.001) narrowing the options of the exposure period of joint statistical analysis. Therefore, we used data from day 2 (48 h of exposure) to quantify and compare seed predation among weed species and habitat types with statistical model fitting (Figure 3).
The binomial model of the weed seed consumption data showed significant differences among weed species, studied years, and their interactions (p < 0.001 for all explanatory variables). There were no differences between the habitat types (p = 0.802), interaction of weed species and habitats (p = 0.353), or the interaction of habitats and years (p = 0.842). Seed consumption was more intensive in 2019 than in 2021 in both habitats (Figure 4). P. rhoeas had the highest consumption levels (p < 0.001 compared to the two other species), followed by A. spica-venti (p < 0.001), and the lowest consumption rate was observed in G. aparine in SNH after 48 h consumption (Figure 4).

4. Discussion

In the present study, we investigate seed predation patterns as one measurement per each one year, on important weed species, G. aparine, P. rhoeas, and A. spica-venti, both inside a winter wheat field and in the adjacent SNH near Gödöllő, Hungary. The contribution of invertebrates as seed predators in our study was in consideration of previous findings by Kiss et al. [49] on the activity density, key mixed feeder species, and their phenology in a winter wheat field and in the adjacent SNHs, in Kartal, Northern Hungary, near our study area. They confirmed the presence of arthropods seed predators, mainly Carabids such as Harpalus and Amara species, in that region. This may indicate the potential role of invertebrates as seed predators in the reported rates of weed seed predation by our study.
Our findings showed the importance of weed seed predation on the soil surface, inside the field crop and in the adjacent SNH in both studied years, where soil dwelling arthropods (as one group of the weed seed predators) may play a role. This finding is in agreement with those reported by Westerman et al. [22], Trichard et al. [56], and Carbonne et al. [57] in studies conducted across Europe, which showed relevant patterns of weed seed predation on the soil surface. We certainly found high intensity (100%) of seed predation in many of the seed cards that may indicate the potentiality of invertebrate seed predators on consuming the assessed weed seeds. This finding is in line with those studies reporting that invertebrates as the most important seed predator group during crop growth [58,59]. Our results could also be supported by those obtained by Jonason et al. [60] who found high weed seed predation rates inside wheat fields. Westerman et al. [15] mentioned that seed predation is an important depletion factor for weed seedbanks, reporting the total seed loss due to seed predation to be from 32 to 70% on weed species Lolium multiflorum in organic wheat fields in the Netherlands. Similarly, and in this context, we expect that the seed banks of the tested weed species will be reduced due to the high levels of seed predation rates occurred in the winter wheat field.
Our study detected significant differences in seed predation levels among weed species across time (years), where the assessed weed seeds were consumed differently. This finding is in accordance with those obtained by Gaba et al. [61] and Moles et al. [62] who demonstrated that seed predation levels vary according to weed species. Meiss et al. [63] also found different seed predation rates between different weed species, with the highest being for Viola arvensis Murray, then Alopecurus myosuroides Huds, and the lowest for Sinapis arvensis L. Although Osman et al. [39] observed seeds of different weed species being similarly consumed, they found seed consumption levels were significantly deferred between years, which is consistent with the findings on Zhang et al. [33] who stated that seed losses caused by seed predators can be substantial and vary between years [15,35,36,44]. The variations in seed predation rates found in our study over the years could be attributed to the different foraging mechanisms and feeding behaviours of the seed predator (carabids) species. For example, Westerman et al. [64] mentioned that some vertebrate species in some cases are quick to respond to changes in seed availability than invertebrate seed predators. Additionally, seed preference and availability of weed seed species and alternative preys as food sources could directly affect seed predation rates.
Our results showed that habitat type, e.g., SNHs versus in-field conditions, did not influenced seed predation levels, as they were found to be similar in both habitats. However, this was contrary to our expectations, as we hypothesized that seed predation levels will vary due to habitat type, which did not happen. This result agreed with those reported by Ichihara et al. [65] who mentioned that seed predation patterns at the field edges were similar to those within the field interior areas. This could be attributed to the presence of same predators’ population or individuals in both habitats, or indicate that both habitats were comfortable and thus preferred by the involved seed predators. However, our results are inconsistent with the findings of González et al. [66], who observed different levels of seed predation across habitat types. This might be related to the positive connections between ecosystem services and seed predator activity density.
This study, although it measured and observed seed predation in specific time (48 h after field exposure), as a single measurement of seed predation in each of the two years, provides findings indicating the potentiality of seed predation on the examined weed species in both habitat types and years, and shows acceptable level of validity, relevance and consistence with most of the previous findings. Our results could thus act as new findings and a report on short-term estimation on weed seed predation in winter wheat fields and adjacent SNHs in Hungary.

5. Conclusions

Our study observed weed seed predation in all investigated seed cards in a winter wheat field and the adjacent SNH, indicating the potentiality of seed predation on the examined weed species. Despite studying a relatively short period of time, 48 h of exposure, it was found appropriate to identify and quantify weed seed predation levels which was assessed once each year. The findings provide a contribution to weed management by reducing the number of exposed weed seeds on the soil surface, thus decreasing the soil weed seed bank, and the number of germinate weed seedlings in the next cropping season. Therefore, weed seed predation should be considered in IWM programs under the integrated pest management framework. This regulation ecosystem service, likely to be delivered by various animals, demonstrates the importance of a system approach (crops, off-crop habitats, trophic levels).

Author Contributions

Conceptualization, M.G.A.O., M.S. and J.K.; Software, Validation, M.S.; Formal analysis, Visualization, M.S.; investigation, M.G.A.O. and M.S.; methodology, M.S., J.K., Z.D. and M.G.A.O.; supervision, Z.D. and M.S.; Resources, M.G.A.O.; writing-original draft preparation, M.G.A.O.; writing-review and editing, M.G.A.O., J.K., M.S., Z.D. and M.Z.; Project administration, J.K. and Z.D.; Funding acquisition, J.K. and Z.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research supported by the Ministry for Innovation and Technology within the framework of Thematic Excellence Program 2020, Institutional Excellence Subprogram (TKP2020-IKA-12) for research on plant breeding and plant protection, The financial fund by the Stipendium Hungaricum scholarship program 2018–2022.

Data Availability Statement

Not applicable.

Acknowledgments

Thanks are extended to student Kovacs Timea, for her help with the field work, and to István Balla, managing director, MATE Non-profit Ltd. (Szárítópuszta), our study area, for allowing us to perform our experiments.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. FAO. Glossary of phytosanitary terms. FAO Plant Prot. Bull. 1990, 38, 5–23. [Google Scholar]
  2. FAO. Glossary of Phytosanitary Terms; ISPM 5; IPPC; FAO: Rome, Italy, 1995; [published 1996]. [Google Scholar]
  3. IPPC. International Plant Protection Convention; IPPC; FAO: Rome, Italy, 1997. [Google Scholar]
  4. CPM. Report of Seventh Session of the Commission on Phytosanitary Measures; IPPC; FAO: Rome, Italy, 2012. [Google Scholar]
  5. Zimdahl, R. Definition of plant competition. In Weed–Crop Competition: A Review, 2nd ed.; Blackwell Publishing Professional: Ames, IA, USA, 2004; pp. 6–8. [Google Scholar]
  6. FAO: Food and Agriculture Organization of the United Nations Statistics Division. Reuters 2021: German Cabinet Approves Legislation to Ban Glyphosate from 2024; FAO: Rome, Italy, 2021. [Google Scholar]
  7. Reuters. Available online: https://www.reuters.com/article/us-germany-farming-lawmakingidUSKBN2AA1GF (accessed on 10 September 2021).
  8. Bohan, D.A.; Boursault, A.; Brooks, D.R.; Petit, S. National-scale regulation of the weed seedbank by carabid predators. J. Appl. Ecol. 2011, 48, 888–898. [Google Scholar] [CrossRef]
  9. Rotteveel, A. Directive 2009/128/EC on the sustainable use of pesticides. In Fourth European Workshop on Standardized Procedure for the Inspection of Sprayers in Europe; SPISE: Lana (South Tyrol), Italy, 2012; pp. 21–27. [Google Scholar]
  10. Altieri, M.A.; Letourneau, D.K. Vegetation management and biological control in agroecosystems. Crop Prot. 1982, 1, 405–430. [Google Scholar] [CrossRef]
  11. Thomas, M.; Wratten, S.; Sotherton, N. Creation of ‘island’ habitats in farmland to manipulate populations of beneficial arthropods: Predator densities and emigration. J. Appl. Ecol. 1991, 28, 906–917. [Google Scholar] [CrossRef]
  12. Collins, K.; Boatman, N.; Wilcox, A.; Holland, J. A 5-year comparison of overwintering polyphagous predator densities within a beetle bank and two conventional hedge banks. Ann. Appl. Biol. 2003, 143, 63–71. [Google Scholar] [CrossRef]
  13. Green, R.; Osborne, P.; Sears, E. The distribution of passerine birds in hedgerows during the breeding season in relation to characteristics of the hedgerow and adjacent farmland. J. Appl. Ecol. 1994, 31, 677–692. [Google Scholar] [CrossRef]
  14. Brust, G.E.; House, G.J. Weed seed destruction by arthropods and rodents in low-input soybean agroecosystems. Am. J. Altern. Agric. 1988, 3, 19–25. [Google Scholar] [CrossRef]
  15. Westerman, P.; Wes, J.; Kropff, M.; Van der Werf, W. Annual losses of weed seeds due to predation in organic cereal fields. J. Appl. Ecol. 2003, 40, 824–836. [Google Scholar] [CrossRef]
  16. Holland, J.M.; Bianchi, F.J.; Entling, M.H.; Moonen, A.C.; Smith, B.M.; Jeanneret, P. Structure, function and management of semi-natural habitats for conservation biological control.: A review of European studies. Pest Manag. Sci. 2016, 72, 1638–1651. [Google Scholar] [CrossRef]
  17. Griffiths, G.J.; Holland, J.M.; Bailey, A.; Thomas, M.B. Efficacy and economics of shelter habitats for conservation biological control. Biol. Control 2008, 45, 200–209. [Google Scholar] [CrossRef]
  18. Firbank, L.; Bradbury, R.B.; McCracken, D.I.; Stoate, C. Delivering multiple ecosystem services from Enclosed Farmland in the UK. Agric. Ecosyst. Environ. 2013, 166, 65–75. [Google Scholar] [CrossRef]
  19. Begg, G.S.; Cook, S.M.; Dye, R.; Ferrante, M.; Franck, P.; Lavigne, C.; Lövei, G.L.; Mansion-Vaquie, A.; Pell, J.K.; Petit, S. A functional overview of conservation biological control. Crop Prot. 2017, 97, 145–158. [Google Scholar] [CrossRef]
  20. Losey, J.E.; Vaughan, M. The economic value of ecological services provided by insects. Bioscience 2006, 56, 311–323. [Google Scholar] [CrossRef] [Green Version]
  21. Garren, J.M.; Strauss, S.Y. Population-level compensation by an invasive thistle thwarts biological control from seed predators. Ecol. Appl. 2009, 19, 709–721. [Google Scholar] [CrossRef]
  22. Westerman, P.R.; Liebman, M.; Menalled, F.D.; Heggenstaller, A.H.; Hartzler, R.G.; Dixon, P.M. Are many little hammers effective? Velvetleaf (Abutilon theophrasti) population dynamics in two-and four-year crop rotation systems. Weed Sci. 2005, 53, 382–392. [Google Scholar] [CrossRef]
  23. Petit, S.; Cordeau, S.; Chauvel, B.; Bohan, D.A.; Guillemin, J.-P.; Steinberg, C. Biodiversity-based options for arable weed management. A review. Agron. Sustain. Dev. 2018, 38, 48. [Google Scholar] [CrossRef] [Green Version]
  24. Sarabi, V. Factors that influence the level of weed seed predation: A review. Weed Biol. Manag. 2019, 19, 61–74. [Google Scholar] [CrossRef]
  25. Hulme, P.; Benkman, C.; Herrera, C.; Pellmyr, O. Granivory. Plant–Animal Interactions: An Evolutionary Approach; Herrera, C.M., Pellmyr, O., Eds.; Blackwell: Oxford, UK, 2002; Volume 26, pp. 132–154. [Google Scholar]
  26. Kolb, A.; Ehrlen, J.; Eriksson, O. Ecological and evolutionary consequences of spatial and temporal variation in pre-dispersal seed predation. Perspect. Plant Ecol. Evol. Syst. 2007, 9, 79–100. [Google Scholar] [CrossRef]
  27. Honěk, A.; Martinkova, Z.; Jarosik, V. Ground beetles (Carabidae) as seed predators. Eur. J. Entomol. 2003, 100, 531–544. [Google Scholar] [CrossRef] [Green Version]
  28. Holland, J.M.; Perry, J.N.; Winder, L. The within-field spatial and temporal distribution of arthropods in winter wheat. Bull. Entomol. Res. 1999, 89, 499–513. [Google Scholar] [CrossRef]
  29. Hough-Goldstein, J.; Vangessel, M.; Wilson, A. Manipulation of weed communities to enhance ground-dwelling arthropod populations in herbicide-resistant field corn. Environ. Entomol. 2004, 33, 577–586. [Google Scholar] [CrossRef]
  30. Cromar, H.E.; Murphy, S.D.; Swanton, C.J. Influence of tillage and crop residue on post-dispersal predation of weed seeds. Weed Sci. 1999, 47, 184–194. [Google Scholar] [CrossRef]
  31. Gallandt, E.R.; Molloy, T.; Lynch, R.P.; Drummond, F.A. Effect of cover-cropping systems on invertebrate seed predation. Weed Sci. 2005, 53, 69–76. [Google Scholar] [CrossRef]
  32. Zhang, J.; Drummond, F.A.; Liebman, M.; Hartke, A. Insect Predation of Seeds and Plant Population Dynamics; Maine Agricultural and Forest Experiment Station Technical Bulletin; University of Maine: Orano, ME, USA, 1997; Volume 163, 32p. [Google Scholar]
  33. Cardina, J.; Norquay, H.M.; Stinner, B.R.; McCartney, D.A. Post-dispersal predation of velvetleaf (Abutilon theophrasti) seeds. Weed Sci. 1996, 44, 534–539. [Google Scholar] [CrossRef]
  34. Tooley, A.; Froud-Williams, R.; Boatman, N.; Hollandj, J. Laboratory studies of weed seed predation by carabid beetles. In Proceedings of the Brighton Crop Protection Conference Weeds, Brighton, UK, 15 November 1999; pp. 571–572. [Google Scholar]
  35. Mittelbach, G.G.; Gross, K.L. Experimental studies of seed predation in old-fields. Oecologia 1984, 65, 7–13. [Google Scholar] [CrossRef]
  36. Hulme, P.E. Post-dispersal seed predation in grassland: Its magnitude and sources of variation. J. Ecol. 1994, 82, 645–652. [Google Scholar] [CrossRef]
  37. Menalled, F.D.; Marino, P.C.; Renner, K.A.; Landis, D.A. Post-dispersal weed seed predation in Michigan crop fields as a function of agricultural landscape structure. Agric. Ecosyst. Environ. 2000, 77, 193–202. [Google Scholar] [CrossRef]
  38. Osman, M.; Szalai, M.; Zalai, M.; Dorner, Z.; Kiss, J. Measurement of post-dispersal invertebrate seed predation of some relevant weed species in maize fields in Hungary: An ecosystem service provided in crop fields contributing to weed management. Plant Prot. Sci. 2022, 58, 351–359. [Google Scholar] [CrossRef]
  39. Davis, A.S.; Daedlow, D.; Schutte, B.J.; Westerman, P.R. Temporal scaling of episodic point estimates of seed predation to long-term predation rates. Methods Ecol. Evol. 2011, 2, 682–890. [Google Scholar] [CrossRef]
  40. Shields, M.W.; Johnson, A.C.; Pandey, S.; Cullen, R.; González-Chang, M.; Wratten, S.D.; Gurr, G.M. History, current situation and challenges for conservation biological control. Biol. Control 2019, 131, 25–35. [Google Scholar] [CrossRef]
  41. Menalled, F.D.; Smith, R.G.; Dauer, J.T.; Fox, T.B. Impact of agricultural management on carabid communities and weed seed predation. Agric. Ecosyst. Environ. 2007, 118, 49–54. [Google Scholar] [CrossRef]
  42. Saska, P.; Van der Werf, W.; De Vries, E.; Westerman, P. Spatial and temporal patterns of carabid activity-density in cereals do not explain levels of predation on weed seeds. Bull. Entomol. Res. 2008, 98, 169–181. [Google Scholar] [CrossRef] [PubMed]
  43. Davis, A.; Raghu, S. Weighing abiotic and biotic influences on weed seed predation. Weed Res. 2010, 50, 402–412. [Google Scholar] [CrossRef]
  44. Baraibar, B.; Carrión, E.; Recasens, J.; Westerman, P.R. Unravelling the process of weed seed predation: Developing options for better weed control. Biol. Control 2011, 56, 85–90. [Google Scholar] [CrossRef]
  45. Hatvani, A.; Kádár, F.; Kiss, J.; Peter, G. Habitat preference of carabids (Coleoptera: Carabidae) in Central Hungary in winter wheat field and in adjacent habitats. IOBC Wprs Bull. 2001, 24, 87–90. [Google Scholar]
  46. Kiss, J.; Kadar, F.; Toth, I.; Kozma, E.; Toth, F. Occurrence of predatory arthropods in winter wheat and in the field edge. Ecologie 1994, 25, 127–132. [Google Scholar]
  47. Kromp, B. Carabid beetles in sustainable agriculture: A review on pest control efficacy, cultivation impacts and enhancement. Agric. Ecosyst. Environ. 1999, 74, 187–228. [Google Scholar] [CrossRef]
  48. Saska, P.; Vodde, M.; Heijerman, T.; Westerman, P.; van der Werf, W. The significance of a grassy field boundary for the spatial distribution of carabids within two cereal fields. Agric. Ecosyst. Environ. 2007, 122, 427–434. [Google Scholar] [CrossRef]
  49. Kiss, J.; Kádár, F.; Kozma, E.; Tóth, I. Importance of various habitats in agricultural landscape related to integrated pest management: A preliminary study. Landsc. Urban Plan. 1993, 27, 191–198. [Google Scholar] [CrossRef]
  50. FAOSTAT. Food and Agriculture Organization of the United Nations Statistics Division; FAO: Rome, Italy, 2020. [Google Scholar]
  51. Ichihara, M.; Maruyama, K.; Yamashita, M.; Sawada, H.; Inagaki, H.; Asai, M. Quantifying the ecosystem service of non-native weed seed predation in traditional terraced paddy fields. Weed Biol. Manag. 2021, 21, 192–201. [Google Scholar] [CrossRef]
  52. Booman, G.C.; Laterra, P.; Comparatore, V.; Murillo, N. Post-dispersal predation of weed seeds by small vertebrates: Interactive influences of neighbor land use and local environment. Agric. Ecosyst. Environ. 2009, 129, 277–285. [Google Scholar] [CrossRef]
  53. Deroulers, P.; Bretagnolle, V. The consumption pattern of 28 species of carabid beetles (Carabidae) to a weed seed, Viola arvensis. Bull. Entomol. Res. 2019, 109, 229–235. [Google Scholar] [CrossRef] [PubMed]
  54. Faraway, J.J. Extending the Linear Model with R: Generalized Linear, Mixed Effects and Nonparametric Regression Models; Chapman and Hall; CRC: New York, NY, USA, 2016. [Google Scholar]
  55. Cleveland, W.S.; Grosse, E.; & Shyu, W.M. Local regression models. In Statistical Models in S; Chambers, J.M., Hastie, T.J., Eds.; Wadsworth & Brooks; Cole: Pacific Grove, CA, USA, 1992; Chapter 8; p. 608. [Google Scholar]
  56. Trichard, A.; Ricci, B.; Ducourtieux, C.; Petit, S. The spatio-temporal distribution of weed seed predation differs between conservation agriculture and conventional tillage. Agric. Ecosyst. Environ. 2014, 188, 40–47. [Google Scholar] [CrossRef]
  57. Carbonne, B.; Bohan, D.A.; Petit, S. Key carabid species drive spring weed seed predation of Viola arvensis. Biol. Control 2020, 141, 104148. [Google Scholar] [CrossRef]
  58. Harrison, S.K.; Regnier, E.E.; Schmoll, J.T. Post dispersal predation of giant ragweed (Ambrosia trifida) seed in no-tillage corn. Weed Sci. 2003, 51, 955–964. [Google Scholar] [CrossRef]
  59. Mauchline, A.; Watson, S.; Brown, V.; Froud-Williams, R. Post-dispersal seed predation of non-target weeds in arable crops. Weed Res. 2005, 45, 157–164. [Google Scholar] [CrossRef]
  60. Jonason, D.; Smith, H.G.; Bengtsson, J.; Birkhofer, K. Landscape simplification promotes weed seed predation by carabid beetles (Coleoptera: Carabidae). Landsc. Ecol. 2013, 28, 487–494. [Google Scholar] [CrossRef]
  61. Gaba, S.; Deroulers, P.; Bretagnolle, F.; Bretagnolle, V. Lipid content drives weed seed consumption by ground beetles (Colopterea, Carabidae) within the smallest seeds. Weed Res. 2019, 59, 170–179. [Google Scholar] [CrossRef]
  62. Moles, A.T.; Warton, D.I.; Westoby, M. Do small-seeded species have higher survival through seed predation than large-seeded species? Ecology 2003, 84, 3148–3161. [Google Scholar] [CrossRef] [Green Version]
  63. Meiss, H.; Le Lagadec, L.; Munier-Jolain, N.; Waldhardt, R.; Petit, S. Weed seed predation increases with vegetation cover in perennial forage crops. Agric. Ecosyst. Environ. 2010, 138, 10–16. [Google Scholar] [CrossRef]
  64. Westerman, P.R.; Borza, J.K.; Andjelkovic, J.; Liebman, M.; Danielson, B. Density-dependent predation of weed seeds in maize fields. J. Appl. Ecol. 2008, 45, 1612–1620. [Google Scholar] [CrossRef]
  65. Ichihara, M.; Maruyama, K.; Yamashita, M.; Sawada, H.; Inagaki, H.; Ishida, Y.; Asai, M. Quantifying the ecosystem service of non-native weed seed predation provided by invertebrates and vertebrates in upland wheat fields converted from paddy fields. Agric. Ecosyst. Environ. 2011, 140, 191–198. [Google Scholar] [CrossRef] [Green Version]
  66. González, E.; Seidl, M.; Kadlec, T.; Ferrante, M.; Knapp, M. Distribution of ecosystem services within oilseed rape fields: Effects of field defects on pest and weed seed predation rates. Agric. Ecosyst. Environ. 2020, 295, 106894. [Google Scholar] [CrossRef]
Figure 1. Seeds of Galium aparine, glued on sandpaper (25/10 cm, p = 60 (kL361 J-Flex Klingspor) (Photo: Osman Mohammed, MATE University, Institute of Plant Protection, Hungary, Gödöllő, 2019).
Figure 1. Seeds of Galium aparine, glued on sandpaper (25/10 cm, p = 60 (kL361 J-Flex Klingspor) (Photo: Osman Mohammed, MATE University, Institute of Plant Protection, Hungary, Gödöllő, 2019).
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Figure 2. Seed cards (covered by wire mesh, hole size—25 mm) placed horizontally inside wheat fields between crop stands (Photo: Osman Mohammed, Hungary, Szárítópuszta, Gödöllő, 2019).
Figure 2. Seed cards (covered by wire mesh, hole size—25 mm) placed horizontally inside wheat fields between crop stands (Photo: Osman Mohammed, Hungary, Szárítópuszta, Gödöllő, 2019).
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Figure 3. Temporal patterns of seed predation of weed species Ap: Apera spica-venti, Ga: Galium aparine, and Pa: Papaver rhoeas, exposed to seed predation inside the winter wheat field and the adjacent SNH in 2019 and 2021, Gödöllő, Hungary. The figure was created based on the daily data collection where the lines are smooth to demonstrate better the trend of change on seed predation. The smoothed trendlines were created by local polynomial regression fitting implemented in R, based on the cloess package of Cleveland et al. [55], to provide an easy-to-grasp descriptive graph of the weed seed consumption.
Figure 3. Temporal patterns of seed predation of weed species Ap: Apera spica-venti, Ga: Galium aparine, and Pa: Papaver rhoeas, exposed to seed predation inside the winter wheat field and the adjacent SNH in 2019 and 2021, Gödöllő, Hungary. The figure was created based on the daily data collection where the lines are smooth to demonstrate better the trend of change on seed predation. The smoothed trendlines were created by local polynomial regression fitting implemented in R, based on the cloess package of Cleveland et al. [55], to provide an easy-to-grasp descriptive graph of the weed seed consumption.
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Figure 4. Seed consumption after 48 h of weed species Ap: Apera spica-venti, Ga: Galium aparine, and Pa: Papaver rhoeas. Seed cards with 20 seeds (n = 40 for one species in one year), were exposed to seed predation inside the winter wheat field and in the adjacent SNH in 2019 and 2021, Gödöllő, Hungary. Boxes graphics represent minimum, maximum, quartiles, and median values, whereas the dots represent outliers. The different alphabet (underlined) letters mean there are significant differences in seed consumption (after 48 h of field exposure) of weed species by habitat types and years.
Figure 4. Seed consumption after 48 h of weed species Ap: Apera spica-venti, Ga: Galium aparine, and Pa: Papaver rhoeas. Seed cards with 20 seeds (n = 40 for one species in one year), were exposed to seed predation inside the winter wheat field and in the adjacent SNH in 2019 and 2021, Gödöllő, Hungary. Boxes graphics represent minimum, maximum, quartiles, and median values, whereas the dots represent outliers. The different alphabet (underlined) letters mean there are significant differences in seed consumption (after 48 h of field exposure) of weed species by habitat types and years.
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Table 1. Percentages of weed seed cards with 100% consumption after 3 to 6 days of exposure to seed predation inside the winter wheat field and in the adjacent SNH in 2019 and 2021, Gödöllő, Hungary.
Table 1. Percentages of weed seed cards with 100% consumption after 3 to 6 days of exposure to seed predation inside the winter wheat field and in the adjacent SNH in 2019 and 2021, Gödöllő, Hungary.
YearWeed SpeciesAfter 3 DaysAfter 4 DaysAfter 5 DaysAfter 6 Days
2019Apera spica-venti25%55%90%NA
Galium aparine8%33%75%NA
Papaver rhoeas73%95%100%NA
2021Apera spica-venti0%3%18%43%
Galium aparine0%0%5%30%
Papaver rhoeas0%0%15%58%
Table 2. Average cumulative consumption (20 initial seeds card-1) (±SD N = 40 for one species in one year) of the assessed weed species after 3–6 days of exposure to seed predation inside the winter wheat field and in the adjacent SNH, in 2019 and 2021 Gödöllő, Hungary.
Table 2. Average cumulative consumption (20 initial seeds card-1) (±SD N = 40 for one species in one year) of the assessed weed species after 3–6 days of exposure to seed predation inside the winter wheat field and in the adjacent SNH, in 2019 and 2021 Gödöllő, Hungary.
YearWeed SpeciesCons. ± SD Day3Cons. ± SD Day4Cons. ± SD Day5Cons. ± SD Day6
2019Apera spica-venti18.35 ± 1.27 a19.50 ± 0.6 A19.9 ± 0.3 αNA
Galium aparine17.10 ± 1.66 a18.95 ± 1.22 A19.75 ± 0.44 αNA
Papaver rhoeas19.62 ± 0.77 b19.95 ± 0.22 A20 ± 0.0 αNA
2021Apera spica-venti15.10 ± 1.37 a17.23 ± 1.23 A18.45 ± 1.04 α19.25 ± 0.74 Ά
Galium aparine14.82 ± 1.43 a16.92 ± 1.12 A18.2 ± 0.85 α19.08 ± 0.73 Ά
Papaver rhoeas15.18 ± 1.24 a16.82 ± 1.13 A18.48 ± 1.04 α19.45 ± 0.75 Ά
Significance classes are indicated with letters. (The different alphabet letters mean there are significant differences in seed consumption of weed species by exposure days and years).
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Osman, M.G.A.; Szalai, M.; Zalai, M.; Dorner, Z.; Kiss, J. Assessing the Importance of Natural Regulating Mechanisms in Weed Management: The Case of Weed Seed Predation in a Winter Wheat Field and in Adjacent Semi-Natural Habitat in Northern Hungary. Agronomy 2022, 12, 2666. https://doi.org/10.3390/agronomy12112666

AMA Style

Osman MGA, Szalai M, Zalai M, Dorner Z, Kiss J. Assessing the Importance of Natural Regulating Mechanisms in Weed Management: The Case of Weed Seed Predation in a Winter Wheat Field and in Adjacent Semi-Natural Habitat in Northern Hungary. Agronomy. 2022; 12(11):2666. https://doi.org/10.3390/agronomy12112666

Chicago/Turabian Style

Osman, Mohammed Gaafer Abdelgfar, Márk Szalai, Mihály Zalai, Zita Dorner, and Jozsef Kiss. 2022. "Assessing the Importance of Natural Regulating Mechanisms in Weed Management: The Case of Weed Seed Predation in a Winter Wheat Field and in Adjacent Semi-Natural Habitat in Northern Hungary" Agronomy 12, no. 11: 2666. https://doi.org/10.3390/agronomy12112666

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