Diet Composition and Significance of Earthworms as Food of Harvestmen (Arachnida: Opiliones).
ABSTRACT.--We gathered dietary data for several harvestman species in a soybean field and adjacent hedgerow habitats to assess the extent of their polyphagy. A total of 1032 harvestmen, predominantly Leiobunum spp., were observed during almost 50 search hours over two seasons. More harvestmen and increased foraging activity were observed in the hedgerow than in the soybean field, and in both habitats harvestmen were more active at night. Earthworms (Oligochaeta: Lumbricidae) were the prey items most frequently recorded as being consumed by all observed harvestman species in both habitats (47.1%), while fruit and other plant material constituted 18.1% of the records. Feeding trials conducted with female harvestmen, Hadrobunus maculosus (Wood), revealed that these arachnids were not capable of subduing live earthworms, suggesting that consumption of these in the field might be limited to scavenging. Implications of harvestman foraging for local food web dynamics are discussed.
Harvestmen (Arachnida: Opiliones) are a ubiquitous yet largely neglected group of arachnids. These facultative predators form a significant component of arthropod communities in woodlands (Todd, 1949; Walker, 1957; Adams, 1984) and agricultural fields (Ashby, 1974; Brust et at., 1986). Several studies further indicate that harvestmen, primarily Phalangium opilio (L), may be significant biocontrol agents of homopteran (Dixon and MeKinlay, 1989), coleopteran (Drummond et at., 1990) and lepidopteran (Ashby, 1974) pests in crop communities. Despite their ubiquity and suggested importance in agricultural systems, detailed knowledge of feeding ecology of harvestmen is lacking. It is generally assumed that harvestmen are predators of smaller invertebrates and opportunistic scavengers of dead animal and plant matter (Bishop, 1949; Todd, 1949, 1950; Phillipson, 1960a; Ashby, 1974). Nevertheless, dietary data for these arachnids are either anecdotal (O'Brien, 1947; Bishop, 1949; Bristowe, 1949; Sankey, 1949; Todd, 195 0) or come from studies designed to evaluate consumption of a specific primarily pest species (Ashby, 1974; Drummond et at., 1990). In order to place these arachnids in a wider ecological context and to assess their potential for reducing pest populations it is crucial to accumulate additional quantitative information on harvestman foraging in a variety of natural and crop communities.
Our objective was to collect data on diet of harvestmen as part of an ongoing project describing generalist predators in agroecosystems. We gathered evidence for the predatory role of harvestmen in a soybean field and its adjacent hedgerow habitat. Preliminary observations found that earthworms were the most frequently observed items in the harvestmen's diet in both habitats. Many earthworms fed upon by harvestmen appeared freshly killed. Bristowe (1949) reported consumption of small live earthworms by harvestmen. Taken together, these findings raised a basic question: Were harvestmen primarily scavenging or also capable of killing earthworms? These two modes of energy acquisition have fundamentally different consequences for the resource. Whereas predators may impact population dynamics of their prey populations, scavenging does not immediately influence the rate of resource renewal in the system. Considering the ecological importance of earthworms in soil formation and conservation processes (Darwin, 1881; Edwards et at., 1995), frequent predation of these oligochaetes may compromise harvestmen's beneficial role in crop communities. To address this question we conducted a feeding experiment to test harvestmen's ability to subdue live earthworms.
MATERIALS AND METHODS
This study was conducted at the Ecological Research Center of Miami University, Oxford, Ohio. Prey selection and feeding behavior of harvestmen were observed in a 0.7 ha soybean field and adjacent hedgerow habitats. Soybean field observations were conducted in a 0.1 ha field area which included approximately 670 m of soybean plants. Hedgerow searches were done on a 160-rn transect along a hedgerow-field edge. Observations were made during 30- to 60-min walks (n = 29) conducted between 08:00 and 11:00 (day search) and between 21:30 and 00:30 from August to September 1997 and June to August 1998. Night searches were conducted with headlamps. During each observation period in both habitats we recorded all harvestmen encountered either on the ground or foliage and their feeding activity. When a feeding event was observed the harvestman with its prey item were collected and preserved in ethyl alcohol; harvestman taxon and food category were then identified in the laboratory.
Because earthworms were the most frequently recorded food items an experiment was carried out to test whether harvestmen were primarily scavenging dead earthworms or whether they were capable of killing them. Fourteen adult females of Hadrobunus maculosus (Wood) were used in the experiment. This is the largest species collected in our study, with females measuring up to 12 mm in body length (excluding legs; Bishop, 1949). We chose H. maculosus due to its large body size and aggressive foraging behavior observed in the field. We hypothesized that if this species is unable to subdue earthworms it is unlikely that smaller species of harvestmen would have this foraging ability.
Harvestmen were field-collected and fed crickets killed by freezing ad lib over a 24-h period and subsequently starved for 7 d before the experiment to equalize their hunger level. Harvestmen were then placed individually in plastic cylindrical experimental arenas (0.066 [m.sup.2] X 12 cm high) with a moist filter paper substrate and one live or dead field-collected juvenile earthworm (Lumbricus sp.), depending on the treatment. Earthworms were killed by freezing (15 mm) and offered to harvestmen thawed.
The average weight of earthworms offered live was 0.46 g [pm] 0.03 SE; (n = 7) and dead 0.40 g [pm] 0.03; (n = 7). Worms of similar size were used in both treatments (t = 1.58; df = 12; P = 0.14). Earthworms used in the experiment were of similar size (4-6 cm) to those consumed by harvestmen in the field; the original body size of subdued earthworms was estimated based on the width of their body fragments collected during searches. Harvestmen were weighed (to 1/10,000 g) immediately before being introduced into experimental arenas and again after 24 h. The experiment was conducted under constant temperature conditions (21C) and a 12L: 12D photoperiod. We used the Wilcoxon signed-rank test for matched pairs to compare pre- and postfeeding body weights of the same individuals, as the data did not conform to assumptions of normality. Data were analyzed with JMP statistical software (SAS Institute, 1997).
RESULTS AND DISCUSSION
A total of 1032 harvestmen were observed during almost 50 search hours over the two seasons. As species determination of these animals in the field is problematic, composition was based on the collection of individuals with prey items. The most frequently collected species consuming food was Leiobunum nigripes Weed (50.7%), followed by L. vittatum (Say) (17.4%), L. politum Weed (9.4%), L. calcar (Wood) (7.3%) and Hadrobunus maculosus (4.4%).
More harvestmen, and a higher proportion of feeding individuals, were observed in the hedgerow than the soybean field and also during the night searches in both habitats (Table 1). Most harvestmen are sensitive to desiccation (Todd, 1949) so the structurally complex hedgerow vegetation likely provided better microclimatic conditions compared to soybeans. Increased harvestman movement and feeding activities frequently observed at night (Sankey, 1949; Todd, 1949; Phillipson, 1960a; Williams, 1962; Edgar and Yuan, 1968) closely relates to increased relative humidity during this period. Our observations also support predominantly nocturnal habits of these arachnids. Higher relative humidity at night may also improve foraging conditions in the soybean field, allowing harvestman dispersal from the hedgerow habitat (Halaj and Cady, pers. obs.).
Harvestmen consumed similar food in both habitats with the exception of fruit, the majority being blackberries (Rubus fruticosus L.) and other plant material, which constituted as much as 25.0% of their consumption in the hedgerow (Table 1). Earthworms were the most frequently recorded prey items of all opilionid species in both habitats, comprising 47.1% of the harvestmen diet (Table 1). The average length of earthworm body segments consumed by harvestmen was 1.3 cm ([pm]1.1 cm; n = 65). The majority of earthworms (83.1%) were transported from the ground and consumed on the vegetation; macerated remains of earthworms were commonly found scattered on the plant surface. Ingestion of food at elevated "feeding stations" may represent an adaptation of harvestmen to alleviate food competition with ground predators such as ants and carabid beetles. A similar feeding behavior was observed by Bristowe (1949). Earthworms were consumed fresh or in various degrees of decomposition. On one occasion we observed a male an d female of Leiobunum nigripes jointly extracting a fresh motionless earthworm from a ground burrow with their chelicerae.
Before being offered food female harvestmen weighed 0.112 g ([pm]0.007; n = 7) and 0.113 g ([pm]0.008; n = 7) in the live and dead earthworm treatments, respectively. Over 24 h, all females confined with dead earthworms gained 11.3% of their body weight ([W.sub.s] = 14.00; P = 0.016). All dead earthworms were found macerated and partly dismembered, further confirming consumption by harvestmen. On the other hand, harvestmen confined with live earthworms lost, on average, 2.7% of their body weight ([W.sub.s] = - 14.00; P = 0.016) and all earthworms in this treatment were alive and without any visible signs of injury at the end of the experiment.
Hadrobunus maculosus was not capable of killing earthworms in the size class which they readily consume in the field, suggesting that our field observations were likely instances of scavenging. Occasional consumption of live earthworms by harvestmen (Bristowe, 1949) may represent feeding on very small or weakened individuals. Nevertheless, we suggest that harvestmen may opportunistically subdue relatively large prey organisms. We observed three females of Leiobunum nigripes killing and consuming large mayfly (Ephemeroptera) imagos (18.13 to 21.25 mm long), which were almost 2.5 times the harvestmen's body size.
Regardless of the foraging manner, consumption of earthworms may have interesting and important implications for harvestman feeding ecology and local food-web dynamics. A classic view of the role of soil detritivores is to assist in decomposition of dead organic matter. The upward trophic connection between the decomposition and grazing subsystems is generally assumed to be limited to nutrient release to primary producers (Swift et al., 1979). Alternatively, soil-litter detritivores may also function as direct food subsidies to animals foraging in grazing food webs (Polis, 1991). Feeding on earthworms described here and elsewhere (Bishop, 1949; Bristowe, 1949), or on other detritivores and fungivores such as Collembola, Isopoda or Diplopoda (Sankey, 1949; Todd, 1950; Phillipson, 1960b; Adams, 1984), may serve as an important source of energy for harvestmen, perhaps modifying their significance as foragers in grazing food webs (e.g., Ashby, 1974; Dixon and McKinlay, 1989). The consumption of fruit or other pl ant material (Bishop, 1949; Bristowe, 1949; Todd, 1950; and results of this study) may have similar trophic implications.
In the current study we did not find enough evidence to conclude that harvestmen are important predators of insect pests in soybeans. They appeared to be opportunistic scavengers, although some consumption might have resulted from predation (Table 1). Small soft-bodied prey such as aphids and lepidopteran larvae or eggs also can be consumed more rapidly, thus lowering the probability of detecting their consumption in the field. In addition, since we did not gather any data on the relative availability of harvestmen prey, our data should be interpreted with caution. Only well-designed experiments, in which harvestman abundance is directly manipulated, can quantify their role of as biocontrol agents and evaluate the relative ecological role of these arachnids in detrital and grazing food webs.
Acknowledgments.--We thank R. G. Holmberg for identifications of selected harvestman specimens in our collection. This research was supported by a State of Ohio Academic Challenge Fellowship to JH and by USDA Grant 94-37311-1189 and Miami University Committee for Faculty Research grant to ABC.
(1.) Present address: Department of Entomology, University of Kentucky, Lexington 40546-0091
ADAMS, J. 1984. The habitat and feeding ecology of woodland harvestmen (Opiliones) in England. Oikos, 42:361-370.
ASHBY, J. W. 1974. A study of arthropod predation of Pieris rapae L. using serological and exclusion techniques. J. Appl. Ecol., 11:419-425.
BISHOP, S. C. 1949. The Phalangida (Opiliones) of New York. Proc. Rochester Acad. Sci., 9:159-235.
BRISTOWE, W. S. 1949. The distribution of harvestmen (Phalangida) in Great Britain and Ireland, with notes on their names, enemies and food. J. Anim. Ecol., 18:100-114.
BRUST, G. E., B. R. STINNER AND D. A. MCCARTNEY, 1986. Predation by soil inhabiting arthropods in intercropped and monoculture agroecosystems. Agric. Ecosyst. Environ., 18:145-154.
DARWIN, C. 1881. The formation of vegetable mould through the action of worms: with special observations on their habits. Murray, London. 326 p.
DIXON, P. L. AND R. G. MCKINLAY. 1989. Aphid predation by harvestmen in potato fields in Scotland. J. Arachnol., 17:253-255.
DRUMMOND, F., Y. SUHAYA AND E. GRODEN 1990. Predation on the Colorado potato beetle (Coleoptera: Chrysomelidae) by Phalangium opilio (Opiliones: Phalangidae). J. Econ. Entomol., 83:772-778.
EDGAR, A. L. AND H. A. YUAN. 1968. Daily locomotory activity in Phalangium opilic and seven species of Leiobunum (Arthropoda: Phalangida). Bios, 39:167-176.
EDWARDS, C. A., P. J. BOHLEN, D. R. LINDEN AND S. SUBLER. 1995. Earthworms in agroecosystems, p. 185-213. In: P. F. Hendrix (ed.). Earthworm ecology and biogeography. CRC Press, Boca Raton. 244 p.
O'BRIEN, M. V. 1947. Observations upon the ecology of the Phalangida of the Chicago area. Bull. Ecol. Soc. Am., 28:61.
PHILLIPSON, J. 1960a. A contribution to the feeding biology of Milopus morio (F) (Phalangida). J. Anim. Ecol., 29:35-43.
-----, 1960b. The food consumption of different instars of Mitopus morio (F) (Phalangida) under natural conditions. J. Anim. Ecol., 29:299-307.
POLIS, G. A. 1991. Complex trophic interactions in deserts: an empirical critique of food-web theory. Am. Nat., 138:123-155.
SANKEY, J. H. P. 1949. Observations on food, enemies and parasites of British harvest-spiders (Arachnida, Opiliones). Entomol. Mon. Mag., 85:246-247.
SAS INSTITUTE. 1997. JMP Statistical Discovery Software. SAS Institute, Cary, North Carolina. 239 p.
SWIFT, M. J., O. W. HEAL AND J. M. ANDERSON. 1979. Decomposition in terrestrial ecosystems. Blackwell Science, Oxford. 372 p.
TODD, V. 1949. The habits and ecology of the British harvestmen (Arachnida, Opiliones), with special reference to those of the Oxford district. J. Anim. Ecol., 18:209-229.
-----, 1950. Prey of harvestmen (Arachnida, Opiliones). Entomol. Mon. Mag., 86:252-254.
WALKER. T. J. 1957. Ecological studies of the arthropods associated with certain decaying materials in four habitats. Ecology, 38:262-276.
WILLIAMS, G. 1962. Seasonal and diurnal activity of harvestmen (Phalangida) and spiders (Araneida) in contrasted habitats. J. Anim. Ecol., 31:23-42.
Feeding observations and number of diet items (n) consumed by harvestmen in hedgerow and adjacent soybean field Hedgerow Soybeans Day Night Day Night Prey category (n) (n) (n) (n) Homoptera Aphididae 1 Fulgoridae 1 2 other 1 Hemiptera 1 Diptera Larvae 1 Adults 4 Coleoptera Carabidae 1 1 1 1 Cicindelidae 1 Lampyridae 1 Scarabaeidae 1 1 Staphylinidae 1 Other 2 Orthoptera 1 Hymenoptera Formicidae 1 3 Vespidae 1 Araneae 2 Diplopoda 1 2 Annelida 10 41 14 Mollusca 4 2 Fruit and nectar 12 1 Other plant material 4 8 Unidentified 1 3 5 Total diet items 32 68 3 35 Person search h 10.5 10.8 12.3 16.2 Total harvestmen observed/h 24.5 31.6 11.1 18.4 % harvestmen feeding 12.5 20.0 2.2 11.7
|Printer friendly Cite/link Email Feedback|
|Author:||HALAJ, JURAJ; CADY, ALAN B.|
|Publication:||The American Midland Naturalist|
|Article Type:||Statistical Data Included|
|Date:||Apr 1, 2000|
|Previous Article:||Atypical Branching of Foxtail (Setaria spp.) Panicles in West-Central Kansas.|
|Next Article:||A Review of Ecological Determinants of Territoriality within Vertebrate Species.|