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Comparison of methods for sampling Thysanoptera on basswood (Tilia americana L.) trees in mixed northern hardwood deciduous forests
Forest Ecology and Management 201 (2004) 327–334 www.elsevier.com/locate/foreco
Comparison of methods for sampling Thysanoptera on basswood (Tilia americana L.) trees in mixed northern hardwood deciduous forests S.M. Wernera,*, E.V. Nordheimb, K.F. Raffaa a
b
Department of Entomology, 345 Russell Laboratories, University of Wisconsin, Madison, WI 53706, USA Department of Statistics and Forest Ecology and Management, University of Wisconsin, Madison, WI 53706, USA Received 10 May 2004; received in revised form 13 July 2004; accepted 15 July 2004
Abstract Canopy arthropods play integral roles in the functioning, biodiversity, and productivity of forest ecosystems. Yet quantitative sampling of arboreal arthropods poses formidable challenges. We evaluated three methods of sampling the introduced basswood thrips, Thrips calcaratus Uzel (Thysanoptera: Thripidae), from the foliage of basswood canopies with respect to statistical variability and practical considerations (legal, economic and logistical accessibility). All three methods involved removal of foliage, which was performed using a pole-pruner, shotgun, and certified tree-climber. We also tested a fourth method, in which the tree-climber enclosed samples in a plastic bag to estimate losses that occur when branches fall to the ground, even though this is often not practical. The climber plus bag and pole-pruning methods obtained the highest numbers of thrips. Mean number of larval thrips did not vary significantly among the three main sampling methods. Site had a stronger effect on the number of larval thrips obtained than on the number of adults. A significant method by site interaction was observed with adults but not larvae. Significant collection date (which corresponds to thrips life stage) by site interaction was also observed. We regressed sampling methods to determine if the number of thrips obtained using one method can be used to predict the number obtained with another. Tree-climber and pole-pruner data were highly predictive of each other, but shotgun data cannot be used to estimate other methods. Pole-pruning is the most cost-effective and legally permissible technique, but is limited to trees with accessible lower branches. The shotgun method is cost-effective and useful in sampling trees at least up to 27 m, but is prohibited close to human activity. The tree-climber is effective and broadly applicable, but incurs the highest costs. This study shows the need to evaluate a variety of techniques when sampling arboreal insects with respect to predictability, pragmatics and life stages. # 2004 Elsevier B.V. All rights reserved. Keywords: Thysanoptera; Sampling methods; Canopy; Tilia americana
* Corresponding author. Present address: DCNR, Forest Pest Management, 208 Airport Drive, 2nd Floor, Middletown, PA 17057, USA. Tel.: +1 717 651 9113. E-mail address: [email protected] (S.M. Werner).
1. Introduction An understanding of the abundance and diversity of canopy arthropods can provide insight into basic
0378-1127/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2004.07.014
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ecosystem processes and biodiversity (Hammond and Miller, 1998; Richardson et al., 1999). Population data may also be used to monitor the impacts of introduced species (Orwig and Foster, 1998), herbivory (Batzer et al., 1995; Jackson, 1996), forest management practices (Schowalter, 1995; Watt et al., 1997; Su and Woods, 2001), and natural or anthropogenic disturbance (Schowalter, 1994). Unfortunately, quantitative sampling of arboreal arthropods poses a number of logistical and statistical challenges. A number of indirect methods have been attempted, such as sampling frass, alternate life stages, and plant injury (Allen et al., 1986; Parker and Skinner, 1993; Zandt, 1994; Liebhold et al., 1995; Liang et al., 1998). However, these methods do not always accurately estimate the targeted life stage, provide only relative estimates, and are not readily amenable to repeated nondestructive sampling (Zandt, 1994; Liang et al., 1998). A variety of direct methods have also been employed, each with certain advantages and disadvantages. Tree felling is commonly used (Shepherd and Brown, 1971; Batzer et al., 1995), but this is destructive, costly, and eliminates the possibility for repeated sampling. Sampling from scaffolding and gondolas is non-destructive, amenable to repeated sampling, and allows direct access for detailed in situ observations. However, these methods are costly (Jackson, 1996), and restricted to certain types of canopies and terrain (Lowman, 2001; Stork, 2001). They likewise restrict the number of tree- or site-level samples, which reduces their applicability to studies of population dynamics and habitat associations. Sampling with a pole-pruner can generate large sample sizes, but also has limitations. Since insects are often clustered in distribution (Kuno, 1991; Pena and Duncan, 1992), methods that only sample the lower portion of the canopy may introduce bias. Sweney and Jones, 1975 sampled branches with a rifle, but the extent to which this method affects absolute arthropod numbers is unknown. Herms et al., 1990 found that a D-vac more effectively sampled adult Hemiptera, but a beating tray was optimal for early instars. Branch disturbance created by beating, D-vac suction, or shooting results in some error. Despite the need to understand issues associated with arboreal insect sampling, relatively few studies have addressed this subject directly, particularly from the perspective of comparison of sampling methods. American basswood, Tilia americana L., is a major component of northern hardwood forests throughout the
northeastern United States and southeastern Canada (USDA FS, 1991). It often occurs in mixed stands, and is associated with red maple, Acer rubrum L., sugar maple, A. saccharum Marsh., northern red oak, Quercus rubra L., eastern hemlock, Tsuga canadensis (L.) Carr., and yellow birch Betula alleghaniensis Britton. Mature trees can grow up to 43 m tall in closed stands, and often have long straight boles lacking lower branches (Burns and Honkala, 1990; USDA FS, 1991). Basswood provides habitat and pollen for wildlife, helps maintain soil quality (Burns and Honkala, 1990) and has several economic uses (Burns and Honkala, 1990; USDA FS, 1991). Recently, forest monitoring in the Great Lakes region has recorded a significant increase in basswood crown dieback, mortality and defoliation (http:// www.na.fs.fed.us/spfo/fhm/index.htm). Thysanoptera, commonly known as thrips, are an important component of forest canopies, and some can cause extensive damage to trees (Lewis, 1973; Parker et al., 1988; Raffa and Hall, 1989; Kolb and Mccormick, 1993; Mound, 1999). At least five species, including three herbivores: Thrips calcaratus Uzel (introduced basswood thrips), Neohydatothrips tiliae (Hood) (native basswood thrips), Taeniothrips inconsequens (Uzel) (pear thrips), and two predators: Leptothrips mali (Fitch) (black hunter thrips) and Aeolothrips melaleucus Haliday, are known to occur on American basswood (Stannard, 1968; Raffa and Hall, 1989; Raffa et al., 1992; Rieske and Raffa, 1996). Only T. calcaratus has been associated with defoliation and dieback in basswood (Raffa and Hall, 1989). T. calcaratus is univoltine and parthenogenic in North America, comprised exclusively of diploid females that reproduce asexually through thelytoky (Ananthakrishnan, 1990). Adults emerge in early spring, feed on developing buds, and oviposit on the undersides of leaf midveins. Emerging larvae feed on foliage for approximately two weeks before dropping to the ground to pupate within earthen cells (Lewis, 1973; Raffa et al., 1992; Rieske and Raffa, 1996; Parker et al., 1992). Our objective was to compare four sampling methods (pole-pruning, shotgun, tree-climbing, and treeclimbing plus bagging) in terms of absolute numbers, statistical variability and economic, legal, and logistical accessibility. We also tested whether correction factors among procedures are applicable when circumstances require multiple methods. This experi-
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ment was conducted as part of a larger study on impacts of the introduced basswood thrips on forest health in the Great Lakes region of North America.
2. Materials and methods The study area consisted of four northern hardwood forest sites in northern Wisconsin (Table 1). Locations ranged from 45.2 to 46.28 north latitude, and from 88.6 to 91.28 west longitude (Table 1). We sampled each site on 11 and 25 May 2001, which correspond to periods when adults and larvae are most abundant, respectively (Raffa et al., 1992). Tree diameter ranged from 17 to 43 cm at 1.5 m height (Table 1). A sample consisted of the outermost three buds or leaf clusters from a small branch. Samples were placed in a plastic bag containing 70% ethanol, and extracted in the laboratory using a suction funnel containing a white 8–12 cup coffee filter. Thrips were removed from the filter with a fine paintbrush and examined under a compound microscope. The following methods were compared for relative numbers of thrips in a given foliage sample: (1) an 1.83 m pole-pruner with up to four additional 1.83 m extensions; (2) a 20-gauge (15.90 mm bore diameter) shotgun; (3) tree-climber, branch allowed to fall to the ground and (4) tree-climber, branch immediately enclosed in plastic bag. Our primary focus was to compare the first three sampling methods. The last method was included to estimate numbers of insects lost due to branch disturbance using other methods, but has limited utility because it is highly laborious and introduces bias in the branches that may be selected for sampling. Eight trees per method were Table 1 Summary of study site locations and diameter of sampled basswood trees in Wisconsin Site
Location
FHMa 4508868 NAMPb #6 NAMP #16 NAMP #14
458440 N, 458180 N, 468280 N, 458510 N,
a
Diameter of sampled trees (cm) 888560 W 888590 W 908210 W 918140 W
33.15, 23.50, 25.47, 20.21,
41.94 20.72 42.95 17.38
FHM refers to a plot that was included in the national USFS Forest Health Monitoring network. b NAMP refers to a plot that was part of the North American Maple Project, a 10-year study to investigate the causes of sugar maple decline.
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sampled during each collection, distributed equally among the four sites. A split plot analysis within PROC MIXED (SAS Institute, 1999) was used to analyze the numbers of T. calcaratus obtained. Fixed effects included site, collection date, and sampling method. Individual trees (two trees/site) were included as a random effect and viewed as the whole plot error term for testing the main effect of site. The residual error was used for testing all other factors, including interactions. Data were analyzed using either the three main sampling methods (shotgun, tree-climber, and pole-pruner) or all four methods. Because we observed a significant effect of collection date, and significant interactions between collection date with site and method (see Section 3), we also analyzed the two time periods separately. Because the first sampling period consisted almost entirely of adults and the second consisted almost entirely of larvae (see Section 3), we limited singledate analyses to the respective dominant life stages. Variance increased with the mean, so a log10(x + 1) transformation was applied to normalize the data. We explored the relationships among methods and the capability of predicting the numbers of thrips that would have been obtained by one method from the numbers obtained using another method. Specifically, numbers of thrips obtained using one of the three main sampling methods were regressed against each other. All pairwise combinations were considered. Regressions were computed separately for adults and larvae. A cost comparison of the methods was performed. Costs were separated into fixed (independent of sampling intensity) and variable (intensity-dependent) costs. Fixed costs included equipment, and variable costs included labor, vehicle rental, and supplies. We also compared the methods based on the costs required to drive to distant study areas, as this is often required for ecological studies. Because driving time is included in the hourly charges of field assistants, and their fees vary substantially with expertise required for each method, we included one scenario involving no travel and one with 200 km round-trip travel.
3. Results We obtained 3047 thrips representing five species (Table 2). Over 99% of these were T. calcaratus. Other
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Table 2 Total numbers and species of Thysanoptera obtained from basswood canopy foliage Species
5/10/01
5/25/01
Adults Larvae Adults Larvae Herbivores Suborder Terebrantia Neohydatothrips tiliae 0 (Hood) Taeniothrips inconsequens 0 (Uzel)a Thrips calcaratus Uzela 547 Predators Suborder Terebrantia Aeolothrips melaleucus Halidaya Suborder Tubillifera Leptothrips mali (Fitch) a
0
6
0
0
0
12
8
105
2365
0
0
3
0
0
0
1
0
Indicates introduced species.
species obtained in low abundance were N. tiliae, T. inconsequens, L. mali, and A. melaleucus. Based on this distribution, we limited our statistical analysis to T. calcaratus. 98% of the T. calcaratus obtained during the first collection were adults, and 96% obtained during the second collection were larvae (Table 2). This pattern was observed for all sampling methods and at all sites. Samples obtained by a tree-climber and bagged before falling to the ground caught an average of 71 thrips per sample, followed by the pole-pruner, treeclimber, and shotgun, which caught about 64, 51 and 40% as many thrips per sample, respectively (Table 3). The shotgun and tree-climber methods caught significantly fewer thrips than the tree-climber with bag method. When adults were considered separately, the pole-pruner method obtained slightly more thrips than the tree-climber with bag method, although this difference was not significant (Table 3). The tree
climber with bag method caught significantly more larvae than the other methods. All methods showed relatively high standard errors. When all four methods were considered across both collection dates, the tree (within site) factor was not significant. The 2Residual Log Likelihood value for tree was significant when evaluated on a chi-squared table. There were significant effects of collection date (P = 0.0001) and sampling method (P = 0.0001). A strong interaction between collection date and site was also observed (P = 0.0003) (Table 4). The site by method interaction was significant overall (P = 0.0420), and when adults were considered separately (P = 0.0107). In addition, there was a significant interaction for site by collection date by method (P = 0.0056). This might be due to the large main effect of method for larvae (P = 0.0017) and by the fact that the site by method interaction was much more pronounced during the first (adult thrips) than second (larvae) collection. Because of the strong effect of collection date, we analyzed the data separately for each insect life stage. There was a significant effect of foliage sampling method on the number of adults (P = 0.0018) and larvae (P = 0.0017) when all four methods were considered. The effect of site was significant for larvae (P = 0.0284) but not for adults (Table 4). The random effect of tree within site was not significant when the three primary methods were compared. The 2Residual Log Likelihood value for tree was significant when evaluated on a chi-squared table. The effects of collection date (P = 0.0001) and sampling method (P = 0.0079) significantly differed in terms of the number of thrips obtained, when numbers of adults and larvae were combined (Table 5). In addition, there was a significant pairwise interaction between collection date and site (P = 0.0001) and a significant method by site interaction (P = 0.0246). Due to the significant main effect of collection date
Table 3 Comparison of mean ( S.E.) T. calcaratus obtained from basswood canopy foliage using four sampling methods Sampling method
Mean/samplea (N = 16)
S.E.
Mean adults/sample 5/10/01 (N = 8)
S.E.
Mean larvae/sample 5/25/01 (N = 8)
S.E.
Shotgun Pole pruner Tree-climber Climber + bag
28.75b 45.75ab 36.12b 71.38a
5.68 10.31 7.90 16.04
11.38a 22.13a 14.50a 20.38a
2.66 6.52 4.70 3.48
46.13 69.38 57.75 122.38
6.72 15.91 10.56 18.63
a
b b b a
Mean thrips/sample within a column followed by the same letter are not significantly different (Tukey’s L.S.D., 95% CI).
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Table 4 Split plot analysis to evaluate fixed effects, considering four methods of sampling thrips in basswood canopies
Table 5 Split plot analysis to evaluate fixed effects, considering three methods of sampling thrips in basswood canopies
Source of variation
P
Source of variation
d.f.
F
P
2 3 1 6 2 3 6
6.24 4.55 178.39 3.14 1.47 15.17 0.34
0.0079 0.0886 0.0001 0.0246 0.2547 0.0001 0.9067
d.f.
F
Overall Method Site Collection datea Method site Method collection date Collection date site Method site collection date
3 3 1 9 3 3 9
17.20 4.53 298.43 2.33 2.59 8.68 3.46
0.0001 0.0894 0.0001 0.0420 0.0730 0.0003 0.0056
Overall Method Site Collection datea Method site Method collection date Collection date site Method site collection date
Adults (5/10/01) Method Site Method site
3 3 9
9.39 4.35 4.31
0.0018 0.0947 0.0107
Adults (5/10/01) Method Site Method site
2 3 6
11.88 4.95 4.17
0.0040 0.0782 0.0336
Larvae (5/25/01) Method Site Method site
3 3 9
9.51 9.27 1.81
0.0017 0.0284 0.1669
Larvae (5/25/01) Method Site Method site
2 3 6
0.85 10.40 0.93
0.4627 0.0233 0.5204
a
a
Collection date refers to adults collected on 5/10/01, and larvae collected on 5/25/01.
Collection date refers to adults collected on 5/10/01, and larvae collected on 5/25/01.
and interactions between collection date with site and method, we analyzed data separately for adults obtained on 10 May and larvae obtained on 25 May. There was a significant site effect on the number of larvae (P = 0.0233), but not on the number of adults obtained. In contrast, there was a significant effect of method on the number of adults (P = 0.0040), but not larvae. There was a significant interaction between method and site for adults (P = 0.0336), but not larvae. The regression analyses indicate that the numbers of thrips obtained by pole-pruner and tree-climber
methods were highly correlated, but neither was correlated with shotgun data (Table 6). This pattern was observed for both adults and larvae. The predictability between methods was highest when pole-pruner data were regressed on tree-climber data for adults (R2 = 0.73) and larvae (R2 = 71). Although the regressions of shotgun data on other methods were higher for adults than larvae, the results for the slope term were never significant at P < 0.05, and thus the shotgun results are not well-predicted by any of the other methods. The economic analysis indicated that pole-pruning was the most cost effective method of sampling
Table 6 Regression of methods used to sample thrips in basswood canopies Methods
F (P > F)
R2
Slope (S.E.)
Intercept (S.E.)
Intercept T (P > T)
Adults (5/10/01) Shotgun vs. pole-pruner Shotgun vs. tree-climber Pole-pruner vs. tree-climber
3.17 (0.13) 5.18 (0.06) 16.33 (0.01)
0.35 0.46 0.73
0.70 (0.39) 0.83 (0.37) 0.83 (0.21)
0.11 (0.51) 0.09 (0.41) 0.04 (0.27)
0.22 (0.84) 0.21 (0.84) 0.15 (0.88)
Larvae (5/25/01) Shotgun vs. pole-pruner Shotgun vs. tree-climber Pole-pruner vs. tree-climber
0.87 (0.39) 1.52 (0.26) 14.58 (0.01)
0.13 0.20 0.71
0.19 (0.20) 0.35 (0.29) 0.56 (0.15)
1.31 (0.36) 1.03 (0.50) 0.74 (0.26)
3.69 (0.01) 2.07 (0.08) 2.84 (0.03)
Pairwise comparisons performed to determine predictabilities among methods and to evaluate applicability of applying a correction factor when more than one sampling method is used.
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Table 7 Economic comparison of methods used to sample basswood canopies for thrips (USD, 2001)a Method
Certified Tree-climber Shotgun
Pole-pruner w/two 1.8 m extensions a
Fixed costs (equipment) ($)
650 250
166
Variable costs (labor, supplies, travel)
$20 h1 driving, set-up $40 h1 climbing $5/box ammunition (30 shells) $8/day + $0.20/1.61 km vehicle rental $1362/month graduate stipend (8.51 h1) $8/day + $0.20/1.61 km vehicle rental $1362/month graduate stipend (8.51 h1)
Avgerage time (h) to collect 30 samples from 10 trees
Cost to collect 30 samples from 10 trees ($) 200 km driving (2.27 h)
No driving
2
105.40
60.00
2
74.32
41.48
1
69.32
27.83
Calculations based on fixed and variable costs for Wisconsin in 2001. Results will vary based on in-house resources, wages and inflation.
foliage, followed by the shotgun and tree climber (Table 7). Tree-climber costs are relatively high due to the equipment costs and higher hourly wages incurred, especially if a certified tree-climber must travel to distant sites. Thus, the absolute and relative differences vary with proximity to the sites. Moreover, these specific fixed and variable costs are likely to vary among agencies, regions, and years, and so are of primarily relative benefit.
4. Discussion These results suggest that the optimal method for sampling canopy insects can vary with the objectives of a given study. For example, if the goal is to obtain the maximum number of insects, the tree-climber with bag method is most effective, as it reduces losses due to branch disturbance (Table 3). However, if it is necessary to sample various sections of the canopy, and the objective is to compare numbers of thrips among trees or sites, the shotgun or tree-climber (unbagged sample) methods might be preferable because of the larger number of samples that can be obtained (i.e., pole-pruners often can only reach the lower sections of the canopy). The final decision would likely incorporate factors such as proximity to human activity, research personnel, and budget (Table 7). Another important consideration is the amount of time required for each method relative to the phenologies of the target species. If it is necessary to sample both multiple trees per site and multiple sites, it may be
difficult to comprehensively sample species that have brief seasonal activity periods by tree-climbing. Treeclimbing is much more time-consuming than other methods, especially when care must be taken not to damage the tree (e.g. climbing spikes may not be permitted). It may be necessary to sample foliar insects using more than one method within the same study, due to factors related to logistics, economics, and legal access. For instance a pole-pruner is unable to reach branches on trees that lack lower branches, and a shotgun may not be permitted close to human activities. If a correction factor can be applied to methods that vary in a statistically predictable way (i.e. no significant interactions among methods and other factors), using different methods can provide increased sample sizes and statistical replication. This study found the tree-climber and pole-pruner methods could predict results between one another, but neither method could predict shotgun samples (Table 6). This might be because these two methods create less branch disturbance than shotgun sampling. In several cases results changed with insect development stage. For instance, site factors significantly affected the number of larvae but not the number of adults. This suggests that there may be lower variability in factors that strongly affect T. calcaratus adults, such as soil type or tree architecture, than factors that affect larvae, such as light exposure. Method affected the number of adults but not larvae obtained using the three primary methods. This may be explained by differences in activity and distribution
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between adult and larval thrips. Larvae are more sessile and appear less selective about feeding sites than adults, which emerge early in the spring and must select the branches where buds have opened first. These parts of the tree tend to be more exposed and to extend further from the main portion crown, thus making them more accessible to the pole-pruner and tree-climber than the shotgun method (where branches are usually selected from a thick clump in the middle of the crown). The decreased mobility and increased visibility of larvae may also increase their susceptibility to natural enemies on foliage. The significant site by method interactions we observed for adults (but not larvae) may likewise reflect differences in mobility and the effects of canopy architecture on their ability to respond and fall off when foliage is disturbed. Caution must be applied in interpreting results of canopy sampling, as all methods have biases and limitations. A clear objective, e.g. obtaining a maximum number of insects vs. making comparisons among sites, is needed for good experimental design. Additionally, recording the precise position in the canopy from which each sample was derived might facilitate comparisons among sampling methods, as insect numbers may vary among strata of the tree canopy (Batzer et al., 1995).
Acknowledgements We thank tree-climber Sean Gere, lab assistant Prima Chambers, UW-Madison, and the Wisconsin Department of Natural Resources for providing assistance in the field. We thank computer consultant Peter Crump, UW-Madison, College of Agricultural and Life Sciences for assisting with data analysis. We thank Sueo Nakahara, USDA Agricultural Research Service, Systematics Entomology Laboratory, Beltsville, MD, for providing taxonomic support. We thank UW Madison professors Michael Adams, Department of Botany, Richard Lindroth, Department of Entomology, Craig Lorimer, Department of Forest Ecology and Management, Daniel Mahr, Department of Entomology and Daniel Young, Department of Entomology, for input on experimental design and manuscript review. The USDA FS Forest Health Monitoring program and the UW-Madison College of Agricultural and Life Sciences provided support for this project.
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Schowalter, T.D., 1995. Canopy arthropod communities in relation to forest age and alternative harvest practices in western Oregon. For. Ecol. Manage. 78, 115–125. Shepherd, R.F., Brown, C.E., 1971. Sequential egg band sampling and probability methods of predicting defoliation by Malacosoma disstria (Lasiocampidae: Lepidoptera). Can. Entomol. 103, 1371–1379. Su, J.C., Woods, S.A., 2001. Importance of sampling along a vertical gradient to compare the insect fauna in managed forests. Environ. Entomol. 30, 400–408. Stannard, L.J., 1968. The thrips or Thysanoptera of Illinois. Illinois Nat. History Survey Bull. 29, 215–552. Stork, N.E., 2001. The management implications of canopy research. Plant Ecol. 153, 313–317. Sweney, W.J., Jones, A.E., 1975. Methods for sampling foliage and insect populations of the beech forest canopy. N.Z. J. For. Sci. 5, 119–122. USDA FS, 1991. Important Forest Trees of the Eastern United States. USDA FS FS-466, 111 pp. Watt, A.D., Stork, N.E., Mcbeath, C., Lawson, G.L., 1997. Impact of forest management on insect abundance and damage in a lowland tropical forest in Southern Cameroon. J. Appl. Ecol. 34, 985–998. Zandt, H.S., 1994. A comparison of three sampling techniques to estimate population size of caterpillars in trees. Oecologia 97, 399–406.
Comparison of methods for sampling Thysanoptera on basswood (Tilia americana L.) trees in mixed northern hardwood deciduous forests S.M. Wernera,*, E.V. Nordheimb, K.F. Raffaa a
b
Department of Entomology, 345 Russell Laboratories, University of Wisconsin, Madison, WI 53706, USA Department of Statistics and Forest Ecology and Management, University of Wisconsin, Madison, WI 53706, USA Received 10 May 2004; received in revised form 13 July 2004; accepted 15 July 2004
Abstract Canopy arthropods play integral roles in the functioning, biodiversity, and productivity of forest ecosystems. Yet quantitative sampling of arboreal arthropods poses formidable challenges. We evaluated three methods of sampling the introduced basswood thrips, Thrips calcaratus Uzel (Thysanoptera: Thripidae), from the foliage of basswood canopies with respect to statistical variability and practical considerations (legal, economic and logistical accessibility). All three methods involved removal of foliage, which was performed using a pole-pruner, shotgun, and certified tree-climber. We also tested a fourth method, in which the tree-climber enclosed samples in a plastic bag to estimate losses that occur when branches fall to the ground, even though this is often not practical. The climber plus bag and pole-pruning methods obtained the highest numbers of thrips. Mean number of larval thrips did not vary significantly among the three main sampling methods. Site had a stronger effect on the number of larval thrips obtained than on the number of adults. A significant method by site interaction was observed with adults but not larvae. Significant collection date (which corresponds to thrips life stage) by site interaction was also observed. We regressed sampling methods to determine if the number of thrips obtained using one method can be used to predict the number obtained with another. Tree-climber and pole-pruner data were highly predictive of each other, but shotgun data cannot be used to estimate other methods. Pole-pruning is the most cost-effective and legally permissible technique, but is limited to trees with accessible lower branches. The shotgun method is cost-effective and useful in sampling trees at least up to 27 m, but is prohibited close to human activity. The tree-climber is effective and broadly applicable, but incurs the highest costs. This study shows the need to evaluate a variety of techniques when sampling arboreal insects with respect to predictability, pragmatics and life stages. # 2004 Elsevier B.V. All rights reserved. Keywords: Thysanoptera; Sampling methods; Canopy; Tilia americana
* Corresponding author. Present address: DCNR, Forest Pest Management, 208 Airport Drive, 2nd Floor, Middletown, PA 17057, USA. Tel.: +1 717 651 9113. E-mail address: [email protected] (S.M. Werner).
1. Introduction An understanding of the abundance and diversity of canopy arthropods can provide insight into basic
0378-1127/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2004.07.014
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ecosystem processes and biodiversity (Hammond and Miller, 1998; Richardson et al., 1999). Population data may also be used to monitor the impacts of introduced species (Orwig and Foster, 1998), herbivory (Batzer et al., 1995; Jackson, 1996), forest management practices (Schowalter, 1995; Watt et al., 1997; Su and Woods, 2001), and natural or anthropogenic disturbance (Schowalter, 1994). Unfortunately, quantitative sampling of arboreal arthropods poses a number of logistical and statistical challenges. A number of indirect methods have been attempted, such as sampling frass, alternate life stages, and plant injury (Allen et al., 1986; Parker and Skinner, 1993; Zandt, 1994; Liebhold et al., 1995; Liang et al., 1998). However, these methods do not always accurately estimate the targeted life stage, provide only relative estimates, and are not readily amenable to repeated nondestructive sampling (Zandt, 1994; Liang et al., 1998). A variety of direct methods have also been employed, each with certain advantages and disadvantages. Tree felling is commonly used (Shepherd and Brown, 1971; Batzer et al., 1995), but this is destructive, costly, and eliminates the possibility for repeated sampling. Sampling from scaffolding and gondolas is non-destructive, amenable to repeated sampling, and allows direct access for detailed in situ observations. However, these methods are costly (Jackson, 1996), and restricted to certain types of canopies and terrain (Lowman, 2001; Stork, 2001). They likewise restrict the number of tree- or site-level samples, which reduces their applicability to studies of population dynamics and habitat associations. Sampling with a pole-pruner can generate large sample sizes, but also has limitations. Since insects are often clustered in distribution (Kuno, 1991; Pena and Duncan, 1992), methods that only sample the lower portion of the canopy may introduce bias. Sweney and Jones, 1975 sampled branches with a rifle, but the extent to which this method affects absolute arthropod numbers is unknown. Herms et al., 1990 found that a D-vac more effectively sampled adult Hemiptera, but a beating tray was optimal for early instars. Branch disturbance created by beating, D-vac suction, or shooting results in some error. Despite the need to understand issues associated with arboreal insect sampling, relatively few studies have addressed this subject directly, particularly from the perspective of comparison of sampling methods. American basswood, Tilia americana L., is a major component of northern hardwood forests throughout the
northeastern United States and southeastern Canada (USDA FS, 1991). It often occurs in mixed stands, and is associated with red maple, Acer rubrum L., sugar maple, A. saccharum Marsh., northern red oak, Quercus rubra L., eastern hemlock, Tsuga canadensis (L.) Carr., and yellow birch Betula alleghaniensis Britton. Mature trees can grow up to 43 m tall in closed stands, and often have long straight boles lacking lower branches (Burns and Honkala, 1990; USDA FS, 1991). Basswood provides habitat and pollen for wildlife, helps maintain soil quality (Burns and Honkala, 1990) and has several economic uses (Burns and Honkala, 1990; USDA FS, 1991). Recently, forest monitoring in the Great Lakes region has recorded a significant increase in basswood crown dieback, mortality and defoliation (http:// www.na.fs.fed.us/spfo/fhm/index.htm). Thysanoptera, commonly known as thrips, are an important component of forest canopies, and some can cause extensive damage to trees (Lewis, 1973; Parker et al., 1988; Raffa and Hall, 1989; Kolb and Mccormick, 1993; Mound, 1999). At least five species, including three herbivores: Thrips calcaratus Uzel (introduced basswood thrips), Neohydatothrips tiliae (Hood) (native basswood thrips), Taeniothrips inconsequens (Uzel) (pear thrips), and two predators: Leptothrips mali (Fitch) (black hunter thrips) and Aeolothrips melaleucus Haliday, are known to occur on American basswood (Stannard, 1968; Raffa and Hall, 1989; Raffa et al., 1992; Rieske and Raffa, 1996). Only T. calcaratus has been associated with defoliation and dieback in basswood (Raffa and Hall, 1989). T. calcaratus is univoltine and parthenogenic in North America, comprised exclusively of diploid females that reproduce asexually through thelytoky (Ananthakrishnan, 1990). Adults emerge in early spring, feed on developing buds, and oviposit on the undersides of leaf midveins. Emerging larvae feed on foliage for approximately two weeks before dropping to the ground to pupate within earthen cells (Lewis, 1973; Raffa et al., 1992; Rieske and Raffa, 1996; Parker et al., 1992). Our objective was to compare four sampling methods (pole-pruning, shotgun, tree-climbing, and treeclimbing plus bagging) in terms of absolute numbers, statistical variability and economic, legal, and logistical accessibility. We also tested whether correction factors among procedures are applicable when circumstances require multiple methods. This experi-
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ment was conducted as part of a larger study on impacts of the introduced basswood thrips on forest health in the Great Lakes region of North America.
2. Materials and methods The study area consisted of four northern hardwood forest sites in northern Wisconsin (Table 1). Locations ranged from 45.2 to 46.28 north latitude, and from 88.6 to 91.28 west longitude (Table 1). We sampled each site on 11 and 25 May 2001, which correspond to periods when adults and larvae are most abundant, respectively (Raffa et al., 1992). Tree diameter ranged from 17 to 43 cm at 1.5 m height (Table 1). A sample consisted of the outermost three buds or leaf clusters from a small branch. Samples were placed in a plastic bag containing 70% ethanol, and extracted in the laboratory using a suction funnel containing a white 8–12 cup coffee filter. Thrips were removed from the filter with a fine paintbrush and examined under a compound microscope. The following methods were compared for relative numbers of thrips in a given foliage sample: (1) an 1.83 m pole-pruner with up to four additional 1.83 m extensions; (2) a 20-gauge (15.90 mm bore diameter) shotgun; (3) tree-climber, branch allowed to fall to the ground and (4) tree-climber, branch immediately enclosed in plastic bag. Our primary focus was to compare the first three sampling methods. The last method was included to estimate numbers of insects lost due to branch disturbance using other methods, but has limited utility because it is highly laborious and introduces bias in the branches that may be selected for sampling. Eight trees per method were Table 1 Summary of study site locations and diameter of sampled basswood trees in Wisconsin Site
Location
FHMa 4508868 NAMPb #6 NAMP #16 NAMP #14
458440 N, 458180 N, 468280 N, 458510 N,
a
Diameter of sampled trees (cm) 888560 W 888590 W 908210 W 918140 W
33.15, 23.50, 25.47, 20.21,
41.94 20.72 42.95 17.38
FHM refers to a plot that was included in the national USFS Forest Health Monitoring network. b NAMP refers to a plot that was part of the North American Maple Project, a 10-year study to investigate the causes of sugar maple decline.
329
sampled during each collection, distributed equally among the four sites. A split plot analysis within PROC MIXED (SAS Institute, 1999) was used to analyze the numbers of T. calcaratus obtained. Fixed effects included site, collection date, and sampling method. Individual trees (two trees/site) were included as a random effect and viewed as the whole plot error term for testing the main effect of site. The residual error was used for testing all other factors, including interactions. Data were analyzed using either the three main sampling methods (shotgun, tree-climber, and pole-pruner) or all four methods. Because we observed a significant effect of collection date, and significant interactions between collection date with site and method (see Section 3), we also analyzed the two time periods separately. Because the first sampling period consisted almost entirely of adults and the second consisted almost entirely of larvae (see Section 3), we limited singledate analyses to the respective dominant life stages. Variance increased with the mean, so a log10(x + 1) transformation was applied to normalize the data. We explored the relationships among methods and the capability of predicting the numbers of thrips that would have been obtained by one method from the numbers obtained using another method. Specifically, numbers of thrips obtained using one of the three main sampling methods were regressed against each other. All pairwise combinations were considered. Regressions were computed separately for adults and larvae. A cost comparison of the methods was performed. Costs were separated into fixed (independent of sampling intensity) and variable (intensity-dependent) costs. Fixed costs included equipment, and variable costs included labor, vehicle rental, and supplies. We also compared the methods based on the costs required to drive to distant study areas, as this is often required for ecological studies. Because driving time is included in the hourly charges of field assistants, and their fees vary substantially with expertise required for each method, we included one scenario involving no travel and one with 200 km round-trip travel.
3. Results We obtained 3047 thrips representing five species (Table 2). Over 99% of these were T. calcaratus. Other
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Table 2 Total numbers and species of Thysanoptera obtained from basswood canopy foliage Species
5/10/01
5/25/01
Adults Larvae Adults Larvae Herbivores Suborder Terebrantia Neohydatothrips tiliae 0 (Hood) Taeniothrips inconsequens 0 (Uzel)a Thrips calcaratus Uzela 547 Predators Suborder Terebrantia Aeolothrips melaleucus Halidaya Suborder Tubillifera Leptothrips mali (Fitch) a
0
6
0
0
0
12
8
105
2365
0
0
3
0
0
0
1
0
Indicates introduced species.
species obtained in low abundance were N. tiliae, T. inconsequens, L. mali, and A. melaleucus. Based on this distribution, we limited our statistical analysis to T. calcaratus. 98% of the T. calcaratus obtained during the first collection were adults, and 96% obtained during the second collection were larvae (Table 2). This pattern was observed for all sampling methods and at all sites. Samples obtained by a tree-climber and bagged before falling to the ground caught an average of 71 thrips per sample, followed by the pole-pruner, treeclimber, and shotgun, which caught about 64, 51 and 40% as many thrips per sample, respectively (Table 3). The shotgun and tree-climber methods caught significantly fewer thrips than the tree-climber with bag method. When adults were considered separately, the pole-pruner method obtained slightly more thrips than the tree-climber with bag method, although this difference was not significant (Table 3). The tree
climber with bag method caught significantly more larvae than the other methods. All methods showed relatively high standard errors. When all four methods were considered across both collection dates, the tree (within site) factor was not significant. The 2Residual Log Likelihood value for tree was significant when evaluated on a chi-squared table. There were significant effects of collection date (P = 0.0001) and sampling method (P = 0.0001). A strong interaction between collection date and site was also observed (P = 0.0003) (Table 4). The site by method interaction was significant overall (P = 0.0420), and when adults were considered separately (P = 0.0107). In addition, there was a significant interaction for site by collection date by method (P = 0.0056). This might be due to the large main effect of method for larvae (P = 0.0017) and by the fact that the site by method interaction was much more pronounced during the first (adult thrips) than second (larvae) collection. Because of the strong effect of collection date, we analyzed the data separately for each insect life stage. There was a significant effect of foliage sampling method on the number of adults (P = 0.0018) and larvae (P = 0.0017) when all four methods were considered. The effect of site was significant for larvae (P = 0.0284) but not for adults (Table 4). The random effect of tree within site was not significant when the three primary methods were compared. The 2Residual Log Likelihood value for tree was significant when evaluated on a chi-squared table. The effects of collection date (P = 0.0001) and sampling method (P = 0.0079) significantly differed in terms of the number of thrips obtained, when numbers of adults and larvae were combined (Table 5). In addition, there was a significant pairwise interaction between collection date and site (P = 0.0001) and a significant method by site interaction (P = 0.0246). Due to the significant main effect of collection date
Table 3 Comparison of mean ( S.E.) T. calcaratus obtained from basswood canopy foliage using four sampling methods Sampling method
Mean/samplea (N = 16)
S.E.
Mean adults/sample 5/10/01 (N = 8)
S.E.
Mean larvae/sample 5/25/01 (N = 8)
S.E.
Shotgun Pole pruner Tree-climber Climber + bag
28.75b 45.75ab 36.12b 71.38a
5.68 10.31 7.90 16.04
11.38a 22.13a 14.50a 20.38a
2.66 6.52 4.70 3.48
46.13 69.38 57.75 122.38
6.72 15.91 10.56 18.63
a
b b b a
Mean thrips/sample within a column followed by the same letter are not significantly different (Tukey’s L.S.D., 95% CI).
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Table 4 Split plot analysis to evaluate fixed effects, considering four methods of sampling thrips in basswood canopies
Table 5 Split plot analysis to evaluate fixed effects, considering three methods of sampling thrips in basswood canopies
Source of variation
P
Source of variation
d.f.
F
P
2 3 1 6 2 3 6
6.24 4.55 178.39 3.14 1.47 15.17 0.34
0.0079 0.0886 0.0001 0.0246 0.2547 0.0001 0.9067
d.f.
F
Overall Method Site Collection datea Method site Method collection date Collection date site Method site collection date
3 3 1 9 3 3 9
17.20 4.53 298.43 2.33 2.59 8.68 3.46
0.0001 0.0894 0.0001 0.0420 0.0730 0.0003 0.0056
Overall Method Site Collection datea Method site Method collection date Collection date site Method site collection date
Adults (5/10/01) Method Site Method site
3 3 9
9.39 4.35 4.31
0.0018 0.0947 0.0107
Adults (5/10/01) Method Site Method site
2 3 6
11.88 4.95 4.17
0.0040 0.0782 0.0336
Larvae (5/25/01) Method Site Method site
3 3 9
9.51 9.27 1.81
0.0017 0.0284 0.1669
Larvae (5/25/01) Method Site Method site
2 3 6
0.85 10.40 0.93
0.4627 0.0233 0.5204
a
a
Collection date refers to adults collected on 5/10/01, and larvae collected on 5/25/01.
Collection date refers to adults collected on 5/10/01, and larvae collected on 5/25/01.
and interactions between collection date with site and method, we analyzed data separately for adults obtained on 10 May and larvae obtained on 25 May. There was a significant site effect on the number of larvae (P = 0.0233), but not on the number of adults obtained. In contrast, there was a significant effect of method on the number of adults (P = 0.0040), but not larvae. There was a significant interaction between method and site for adults (P = 0.0336), but not larvae. The regression analyses indicate that the numbers of thrips obtained by pole-pruner and tree-climber
methods were highly correlated, but neither was correlated with shotgun data (Table 6). This pattern was observed for both adults and larvae. The predictability between methods was highest when pole-pruner data were regressed on tree-climber data for adults (R2 = 0.73) and larvae (R2 = 71). Although the regressions of shotgun data on other methods were higher for adults than larvae, the results for the slope term were never significant at P < 0.05, and thus the shotgun results are not well-predicted by any of the other methods. The economic analysis indicated that pole-pruning was the most cost effective method of sampling
Table 6 Regression of methods used to sample thrips in basswood canopies Methods
F (P > F)
R2
Slope (S.E.)
Intercept (S.E.)
Intercept T (P > T)
Adults (5/10/01) Shotgun vs. pole-pruner Shotgun vs. tree-climber Pole-pruner vs. tree-climber
3.17 (0.13) 5.18 (0.06) 16.33 (0.01)
0.35 0.46 0.73
0.70 (0.39) 0.83 (0.37) 0.83 (0.21)
0.11 (0.51) 0.09 (0.41) 0.04 (0.27)
0.22 (0.84) 0.21 (0.84) 0.15 (0.88)
Larvae (5/25/01) Shotgun vs. pole-pruner Shotgun vs. tree-climber Pole-pruner vs. tree-climber
0.87 (0.39) 1.52 (0.26) 14.58 (0.01)
0.13 0.20 0.71
0.19 (0.20) 0.35 (0.29) 0.56 (0.15)
1.31 (0.36) 1.03 (0.50) 0.74 (0.26)
3.69 (0.01) 2.07 (0.08) 2.84 (0.03)
Pairwise comparisons performed to determine predictabilities among methods and to evaluate applicability of applying a correction factor when more than one sampling method is used.
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Table 7 Economic comparison of methods used to sample basswood canopies for thrips (USD, 2001)a Method
Certified Tree-climber Shotgun
Pole-pruner w/two 1.8 m extensions a
Fixed costs (equipment) ($)
650 250
166
Variable costs (labor, supplies, travel)
$20 h1 driving, set-up $40 h1 climbing $5/box ammunition (30 shells) $8/day + $0.20/1.61 km vehicle rental $1362/month graduate stipend (8.51 h1) $8/day + $0.20/1.61 km vehicle rental $1362/month graduate stipend (8.51 h1)
Avgerage time (h) to collect 30 samples from 10 trees
Cost to collect 30 samples from 10 trees ($) 200 km driving (2.27 h)
No driving
2
105.40
60.00
2
74.32
41.48
1
69.32
27.83
Calculations based on fixed and variable costs for Wisconsin in 2001. Results will vary based on in-house resources, wages and inflation.
foliage, followed by the shotgun and tree climber (Table 7). Tree-climber costs are relatively high due to the equipment costs and higher hourly wages incurred, especially if a certified tree-climber must travel to distant sites. Thus, the absolute and relative differences vary with proximity to the sites. Moreover, these specific fixed and variable costs are likely to vary among agencies, regions, and years, and so are of primarily relative benefit.
4. Discussion These results suggest that the optimal method for sampling canopy insects can vary with the objectives of a given study. For example, if the goal is to obtain the maximum number of insects, the tree-climber with bag method is most effective, as it reduces losses due to branch disturbance (Table 3). However, if it is necessary to sample various sections of the canopy, and the objective is to compare numbers of thrips among trees or sites, the shotgun or tree-climber (unbagged sample) methods might be preferable because of the larger number of samples that can be obtained (i.e., pole-pruners often can only reach the lower sections of the canopy). The final decision would likely incorporate factors such as proximity to human activity, research personnel, and budget (Table 7). Another important consideration is the amount of time required for each method relative to the phenologies of the target species. If it is necessary to sample both multiple trees per site and multiple sites, it may be
difficult to comprehensively sample species that have brief seasonal activity periods by tree-climbing. Treeclimbing is much more time-consuming than other methods, especially when care must be taken not to damage the tree (e.g. climbing spikes may not be permitted). It may be necessary to sample foliar insects using more than one method within the same study, due to factors related to logistics, economics, and legal access. For instance a pole-pruner is unable to reach branches on trees that lack lower branches, and a shotgun may not be permitted close to human activities. If a correction factor can be applied to methods that vary in a statistically predictable way (i.e. no significant interactions among methods and other factors), using different methods can provide increased sample sizes and statistical replication. This study found the tree-climber and pole-pruner methods could predict results between one another, but neither method could predict shotgun samples (Table 6). This might be because these two methods create less branch disturbance than shotgun sampling. In several cases results changed with insect development stage. For instance, site factors significantly affected the number of larvae but not the number of adults. This suggests that there may be lower variability in factors that strongly affect T. calcaratus adults, such as soil type or tree architecture, than factors that affect larvae, such as light exposure. Method affected the number of adults but not larvae obtained using the three primary methods. This may be explained by differences in activity and distribution
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between adult and larval thrips. Larvae are more sessile and appear less selective about feeding sites than adults, which emerge early in the spring and must select the branches where buds have opened first. These parts of the tree tend to be more exposed and to extend further from the main portion crown, thus making them more accessible to the pole-pruner and tree-climber than the shotgun method (where branches are usually selected from a thick clump in the middle of the crown). The decreased mobility and increased visibility of larvae may also increase their susceptibility to natural enemies on foliage. The significant site by method interactions we observed for adults (but not larvae) may likewise reflect differences in mobility and the effects of canopy architecture on their ability to respond and fall off when foliage is disturbed. Caution must be applied in interpreting results of canopy sampling, as all methods have biases and limitations. A clear objective, e.g. obtaining a maximum number of insects vs. making comparisons among sites, is needed for good experimental design. Additionally, recording the precise position in the canopy from which each sample was derived might facilitate comparisons among sampling methods, as insect numbers may vary among strata of the tree canopy (Batzer et al., 1995).
Acknowledgements We thank tree-climber Sean Gere, lab assistant Prima Chambers, UW-Madison, and the Wisconsin Department of Natural Resources for providing assistance in the field. We thank computer consultant Peter Crump, UW-Madison, College of Agricultural and Life Sciences for assisting with data analysis. We thank Sueo Nakahara, USDA Agricultural Research Service, Systematics Entomology Laboratory, Beltsville, MD, for providing taxonomic support. We thank UW Madison professors Michael Adams, Department of Botany, Richard Lindroth, Department of Entomology, Craig Lorimer, Department of Forest Ecology and Management, Daniel Mahr, Department of Entomology and Daniel Young, Department of Entomology, for input on experimental design and manuscript review. The USDA FS Forest Health Monitoring program and the UW-Madison College of Agricultural and Life Sciences provided support for this project.
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