Institute of Ecology, University of Georgia, Athens GA, 30602
KEY WORDS Biodiversity, parasitoid wasps, latitude, species richness, Ichneumonidae, old-growth forests
Because the forces governing the distribution and abundance of parasitoids are poorly defined, the processes that determine the relationship between species richness and latitude are unclear (Hawkins, Shaw and Askew, 1992). In contrast to the Ichneumonidae, other parasitic families such as the Chalcididae (Hespenheide 1979) and the Encyrtidae (Noyes 1989) appear to be more speciose in the tropics. Janzen (1981) proposed that as one approaches the equator, habitat becomes increasingly patchy with increased floral diversity (Pianka 1966, Stevens 1989). Thus hosts become scarce, and generalist parasitoids are more predominant. Janzen (1981) predicted fewer specialist ichneumonids in the tropics. In addition to general considerations of latitudinal trends (Pianka 1966, Stevens 1989), it has been suggested that resource fragmentation (Janzen 1981, Janzen and Pond 1975, Askew and Shaw 1986, Hawkins 1990, Sime and Brower 1998), plant-host-parasitoid interactions (Hawkins and Lawton 1987; Gauld,Gaston and Janzen 1992), competition (Hawkins, 1990), predation (Rathcke and Price 1976) and environmental factors (Townes, 1972a; Hawkins, 1990; Gauld, 1991; Hawkins et al.1992) influence parasitoid diversity.
Janzen (1981) analyzed published distribution maps of 1,717 North American ichneumonid species and concluded that their peak species richness lies at mid-latitudes between 38° and 42° N. On the east coast, for instance, his analysis suggested that species richness within the latitudes of peak diversity from central Virginia to central New York is 1.5 times higher than in central Georgia and 2.5 higher than in central Florida. He further predicted fewer species of ichneumonids per host species as one approaches the equator, with proportionately fewer species of tropical specialists.
More recently, Gauld (1986, 1987, 1991) and Gaston and Gauld (1993) have examined latitudinal trends for a number of subfamilies within the Ichneumonidae. Their results are equivocal. Some subfamilies appear more diverse in the tropics; others, in temperate areas. Gauld (1986) presented evidence that Australian collections have a slight decrease in the overall ichneumonid diversity nearer the equator. This is in part because of the absence in northern Australia of taxa such as the Ctenopelmetinae that feed on sawflies -- a relatively rare taxa in the tropics. Gauld examined the fauna in 2 tribes of Cryptinae (=Phygadeuontinae) and 9 other subfamilies. As a proportion of this fauna, he reported that the Mesostenini and Pimplinae have more species in the tropical regions of Australia than statistically expected. In contrast, the Labeninae, Anomaloninae and Ctenopelmatinae are significantly more speciose in the temperate regions. Gauld (1987) examined latitudinal trends in the species richness and relative proportion of 5 major ichneumonid taxa (Ctenopelmatinae, Campopleginae, Ophioninae, Mesostenini and Pimplini) in Kevo, Finland (70° N), Leicester, England (53° N), Okinawa (27° N), Santa Rosa National Park, Costa Rica (11° N) and the Ulu Temburong region, Brunei (4° N). He reported higher diversity for the Mesostenini, Pimplini and Ophioninae towards the equator and lower diversity of sawfly parasitoids away from it. Gauld (1991) presented data on the lower pimpliform subfamilies from an extensive survey of Costa Rica that includes 17 sites and over 100 Malaise trap-years. This monograph and the later analysis of Gaston and Gauld (1993) focused on the Pimplinae and, to a lesser extent, the Rhyssinae. Their data show that both local and regional richness of these wasps is generally higher in the tropics than elsewhere.
Weighing the relative importance of factors that govern parasitoid community composition as a function of latitude is difficult. It requires comparable diversity estimates between locations. Unfortunately, few studies have employed the same sampling methods across large geographic areas to obtain comparable site or regional diversity estimates. With speciose taxa, estimates of species richness generally increase with sampling effort (Colwell and Coddington 1994). Well collected areas can be expected to yield higher estimates of species richness than poorly collected areas. Janzen's (1981) finding that North American ichneumonid species richness lies at mid-latitudes and a similar finding by Quicke and Kruft (1995) for the Braconidae are based on published records over large geographic areas. Such results may be an artifact of major collections being within these latitudes and not from underlying biological processes. The current study was designed to overcome this methodological problem. We examine species diversity of two ichneumonid subfamilies along a latitudinal gradient in eastern North America using Malaise traps as a standard sampling technique at five sites from Ontario to Florida.
We examined two subfamilies representative of idiobiont and koinobiont parasitoids (Askew and Shaw, 1986). The Campopleginae are an abundant group of koinobiont endoparasitoids; hosts are mostly Lepidoptera, Symphyta and a few attack Coleoptera (Wahl, 1993). The Ichneumoninae attack lepidopterous hosts exclusively (Gauld 1988). Most are idiobiont endoparasitoids attacking the pupal stages, while others are koinobiont endoparasitoids attacking final-instar larvae (Wahl, 1993). They include the most successful group of idiobiont endoparasitoids within the Ichneumonidae.
Sites. We sampled in five old-growth forests to minimize successional effects. Our latitudinal gradient ranged from 45° 42"N to 29° 44"N. We focused on the latitude of peak species richness for ichneumonids as reported by Janzen (1981). Sites included the Shaw Woods approximately 10 km north of Eganville, Ontario, Renfrew County, (45° 42"N 77° 4"W) which stands on well drained, gravelly sediments deposited by retreating ice sheets in the Great Lakes St. Lawrence Forest Region dominated by Fagus grandifolia Ehrhart (American beech) (Dugal, 1980); Patuxent Wildlife Research Center, Laurel, Prince Georges County, Maryland (39°03"N 76° 49"W) dominated by F. grandifolia Ehrhart; the Hitchiti Experimental Forest, Juliette, Jones County, Georgia in the Peidmont (33° 03" N 83° 43"W) dominated by Ostrya virginiana (Miller) K. Koch (eastern hophornbeam), Acer rubra L. (red maple), Ulmus alata Michaux (winged elm), Querqus alba L. (white oak), and Lirodendron tulipifera L. (yellow poplar); the Tall Timbers Research Station, Tallahassee, Leon County, Florida in the Coastal Plain (30° 39"N 84° 15"W) dominated by F. grandifolia Ehrhart american beech) and Magnolia grandiflora L. (southern magnolia); and the San Felasco Hammock, Gainsville, Alachua County, Florida, a 6,500-acre preserve with climax mesic hammok located in the Coastal Plain (29° 44" N 82° 27"W). Based on work by Dugaul, Lockard (1995, Appendix 1) presented a list of flora for Shaw Woods with site descriptions. Hotchkiss and Stewart (1947) described the Patuxent site, including a species list. Lockard, (1995, Appendix 2) presented a detailed species list of trees at Hitchiti. Hirsch (1981) described the Tall Timbers site near the Woodyard Hammock. Dunn (1982) outlined a detailed description of the San Felasco Hammock.
Sampling. We collected comparable samples across sites for one season in 1993 using fine mesh (.33 mm) Townes-style Malaise traps (Townes 1972) purchased from Sante Traps, (street??, Lexington, KY ZIP). Malaise traps are meshed fabric, open-sided, tent-like structures designed to collect flying insects in 70% ethanol (Owen, 1991). We ran two traps at each site. The traps faced North-South, with the collecting head towards the southern end. Collaborators serviced each trap weekly throughout the period of flight activity, except late or early in the season when they collected some samples biweekly or monthly. We sampled Shaw Woods and Patuxent for an additional season in 1992. We present data from specimens collected from Shaw Woods (May 6-October 22, 1992; May 6-October 21,1993), Patuxent (April 6- November 9, 1992; April 12-October 25, 1993), Hitchiti (March 23-December 21 1993), Tall Timbers (March 30-December 14, 1993) and San Felasco (March 15-December 18, 1993). Tall Timbers included one sample in 1994 (March 4-28, 1994) because we missed the first part of the flight season in 1993.
Specimen Preparation. We mounted all Hymenoptera with 3 or more wing cells. We assigned each specimen a conventional label, and a unique barcode identifier linking that specimen to the database containing location, trap number, and sample dates. See Wayman (1994) for a detailed description of sorting techniques.
Sorting. We sorted all ichneumonids to subfamily. We identified all the ichneumonines and the campoplegines to morphospecies. The genera Dusona and Casinaria were identified to species whenever possible using available taxonomic literature (Heinrich, 1960, 1961, 1962 and 1977; Walley, 1940) and the resources of the American Entomological Institute (AEI) in Gainsville, Florida. We deposited specimens at the University of Georgia and the AEI. The internet address to access the database is http://dial.pick.uga.edu. D. Wahl confirmed that specimens separated simply as morphospecies 1, 2, 3, etc. were separate species.
Minimum Number of Species. The sexual dimorphism in some groups, particularly the Ichneumoninae, made the association of sexes impractical. To calculate the minimum number of species at a site and across sites, we counted only one sex of taxa where we could not associate males and females of a particular genus. For example, in the genus Protichneumon (Ichneumoninae) we identified two species, Protichneumon_sp_San_Felasco_Male_1 and Protichneumon_sp_San_Felasco_Female_2 (Appendix 4, Lockard, 1995). We could have reported 2 species of Protichneumon. Instead we counted the minimum number of one species in the genus Protichneumon. This eliminated the possibility of overestimating numbers of species in any given genus. For details of how this list was constructed see Lockard (1995).
Statistical Estimators. We conducted a statistical analysis using SPLUS (Becker, 1988) to estimate trapping efficiency. We included 5 models for species estimations: Eadie-Hofstee, Chao 1 and 2 (Chao, 1984), Jackknife 1-5 (Burnham and Overton, 1978, 1979), Lamas (Lamas, Robbins and Harvey, 1991), and the Ratio Method (Bailey, 1952) reviewed by Colwell and Coddington (1994). We analyzed 1993 data from all five sites including each trap separately and the two traps combined. We analyzed data from the minimum species list to compare results with the minimum raw number of species. For a between year comparison,we also compared trap catches between 1992 and 1993 from Shaw Woods and Patuxent. To examine whether two traps in the same year yielded the same results as running one trap one year and one the following year, we compared the between-trap and between-year variance at these two sites. Figure 1 shows an example.
Estimates of Species Richness. For each site on both subfamilies we generated estimates of species richness by the Eadie-Hofstee, Lamas et al., Chao1 and Chao2 methods and species accumulation to effort relationship. We give a graphical representation (Figure 1) of the species accumulation effort for Campopleginae at Hitchiti Traps 213 and 214 in 1993. The solid line represents the average number of species as a function of sampling effort. The raw data were randomized 100 times and the mean was then plotted as the solid line. For example, first one sample was taken randomly from the 56 total samples. The number of species in that one sample was calculated. Then, another sample was chosen randomly and the number of species in it calculated. This was done 100 times and the mean was then plotted for sampling effort of one. Next, two samples were chosen randomly, and the number of species in these two was calculated. Again, this was done 100 times and the mean number of species in two samples was thus calculated and graphed. This was done through sampling effort of 56. This solid line thus represents the mean species richness as a function of numbers species. 65% of the data fall within one standard deviation of the mean.
Figure 1 has not reached an asymptote. Without the use of statistical estimators, this indicates we need more data from both sites to determine total species richness. Table 1 present 1993 raw data and 5 species estimates for the Campopleginae and Ichneumoninae respectively. For total species richness at each site, the rank order of the Campopleginae species estimates was consistent with the rank order of the raw data with both traps combined (Hitchiti 1st, Patuxent and San Felasco 2nd, Tall Timbers 3rd, Shaw Woods 4th). There was one exception with the inversion of the second and third place order of Tall Timbers 2nd and Patuxent 3rd using the Chao2 estimate. For certain data sets, particularly the small Campopleginae samples from Shaw Woods, the Chao (Chao, 1984) estimator was inappropriate. The results for these data sets were not available and are denoted by NA. The rank orders for the Ichneumoninae were more variable with both traps combined. Patuxent was ranked 1st in total species richness for the raw data and all estimators, except Nc2 (Chao, 1984) ranked it 2nd. San Felasco was ranked 2nd for all the estimators except Nl (Lamas et. al, 1991) ranked it 3rd. The 3rd, 4th and 5th ranks fluctuated widely between the estimators suggesting little difference in the raw data between Shaw Woods, Tall Timbers, and Hitchiti (Table 1).
Between Year Comparison. Figures 1 and 2 give a graphical representation of the statistical estimators and randomized data for Campopleginae collected at Hitchiti Traps 1 and 2, 1993 and Patuxent Traps 1 and 2, 1992 and 1993. In Figure 1 Hitchiti has a higher estimate of campoplegines than Patuxent. After 2 years and 120 samples, Patuxent (Figure 2) has not reached the over all species richness of Hitchiti with only 1 year and 60 samples. In Figure 1 none of the estimators show any signs of leveling off, indicating we need more data from Hitchiti. The combined 1992 and 1993 data show a flat curve for these 2 estimators, indicating we adequately sampled campopleginae at Patuxent (Figure 2). Therefore, estimates of campoplegine richness at Hitchiti are higher in one year (and still increasing) than Patuxent which leveled off with approximately 44 to 47 species. The Eadie-Hofstee estimator increases dramatically showing no signs of leveling off for both sites.
Collecting Bias. Table 2 presents the fraction deviating from the most speciose site for all sites for the raw data and Janzen's (1981) data. We collected less than half the number of species in Shaw Woods than at Patuxent, the most speciose site. Janzen (1981), for the equivalent latitude at Shaw Woods, reported 95% of his most diverse latitude. Below his most speciose latitude, there is a rapid drop off in the percentage of species collected compared to the most species rich latitude. However, our data show an increase in the percentage of species collected from the most species rich site in Patuxent (Table 2). We suspect that collections around and north of Patuxent are more complete than those south of there, or we under collected at Patuxent. This could explain why Janzen (1981) predicted an almost two-fold drop in species richness between the Patuxent and Hitchiti sites.
One year of data. We may be faulted for having only one year of data for all five sites. It is our hypothesis that with additional trapping years one continues to collect more and more rare species that are random events resulting from the capture of transients. Many of these individuals may not be using the habitat or only passing through it (Wayman, 1994, Gaasch,1995). Gaasch (1995) found transients in many different successional habitats, with concentrations of specimens in a given species found mainly in habitats most suitable for that species. Therefore, we can be confident that common species may be collected in a given year in a particular habitat.
There were exceptions to this finding. The ichneumoninae Diphyus comes (Cresson) contained 41 male specimens in 1993 and none were collected in 1992. We found a similar result with another ichneumonine Setanta compta (Say) with 21 male specimens collected in 1992 and none in 1993. We collected no females of either species in either 1992 or 1993. We can only hypothesize that their biologies may be similar causing yearly variations in abundance because of host switching or unknown reasons.
At both sites in Florida however, we collected a minimum of 53 Ichneumonines in one season, which represents 71% of the 75 known species of Ichneumoninae in Florida (Heinrich, 1977). One year of data represents almost three quarters of the known species at this site. We would also expect higher between-year differences in species diversity because of variation in host population cycles in northern temperate regions. By comparing a single trapping year we eliminated unusually high species richness estimations in this area.
Estimates of Species Richness Still Rising
Standard Methods. Clearly, malaise traps do not collect all species at a given site, yet they have
been documented for their efficiency in collecting Hymenoptera, particularly in the parasitoid
superfamily Ichneumonoidea (Matthews and Matthews, 1970; Owen, Townes and Townes, 1981;
Darling and Packer, 1988; and Noyes, 1989). Although additional trapping data would permit
more accurate estimates of the total species richness at each site, we are generally comfortable with
the trends that they present in terms of the relative abundance of species along the gradient. The
species richness for both subfamilies peaks at mid-latitudes and is lower at the Canadian and
Floridian Sites. Based on the analysis presented, we are fairly confident that the Campopleginae
are more speciose at Hitchiti than at the other sites. Though we appear to have sampled a lower
proportion of the possible ichneumonine diversity, and hence, are less confident in the strength of
our finding for this taxon, it appears that ichneumonine diversity is higher at Maryland than
elsewhere, confirming Janzen's (1981) study.
Study Organisms. Trends reported here may be representative of the two subfamilies, Campoplegine and Ichneumoninae, and not the Ichneumonidae as a whole. Janzen (1981) examined the distributions of eight subfamilies, while our study may be faulted for only examining two. [More specialist in hitchiti than in Patuxent]
Need more studies of subfamilies + sample size
Why Peak in Mid-Latitudes? In the most northern regions, climatic and habitat constraints significantly limit the ability for high diversity of hosts and, in turn, parasitoids. The temperate regions of the Mid-Atlantic states provide more vegetational diversity and host diversity, allowing for maximum parasitoid packing in these areas. Continuing toward the Southeastern states, little change is seen in the piedmont areas from the Mid-Atlantic states in terms of decreasing suitable habitat for maximum parasitoid richness. The lack of sufficient collecting in these areas may not have shown this trend previously. When moving to more tropical environments, the host density decreases to a point that hinders the ability for a tremendous parasitoid load (Janzen,1981).
Gauld and Gaston (1992), offered the "nasty" host hypothesis as a plausible explanation for the decrease in tropical parasitoid diversity. This hypothesis supposes that an increase in secondary plant compounds in tropical plants (Levin 1976), hinders the proliferation of parasitoid species in tropical regions. Parasitoids preying on hosts that feed on less toxic components of plant material are less likely to be affected by this proposed hypothesis. This hypothesis may or may not be a plausible explanation for a drop in species richness in the subtropical Floridian sites. We have no data to either support or reject it.
Heinrich (1977) suggests an ecological, particularly climatic, explanation for a decrease in the Floridian ichneumonines. He states that the Ichneumoninae have proliferated in moderate and cool climates, and Florida with its subtropical climate is much less suitable for high ichneumonine diversity. The weather analysis in Lockard (1995) showed little correlation of parasitoid flight activity with moisture, although, temperature may have some effect on total diversity between sites. We suggest that parasitoid activity declines with average temperatures above 80°F or more. The Floridian climate cannot support many ichneumonine genera that hibernate as adult females (such as Ichneumon, Stenichneumon, Aoplus, Chasmias, Spilichneumon, and Eutanyacra (Heinrich, 1960)). In contrast, the Canadian site with a short flight season may not support species that require longer developmental times or require hosts that are not in Canada. The Patuxent site has both warm summers and harsh winters allowing for maximum species packing at this latitude. The Hitchiti site may be more diverse than previously thought for similar reasons.
Conclusions. In conclusion, these data are consistent with the hypothesis of maximum ichneumonid species richness occurring at mid-latitudes. However, we hypothesize that the peak diversity of ichneumonid parasitoids comprises a wider band than previously reported. Our data suggest that ichneumonid species richness occurs in a broad swath from at least Maryland to Piedmont Georgia, dropping in the south near the coastal plain and in the north near Canada. How far the peak band stretches into upstate New York is unknown. We feel the almost two fold drop in species richness from 37.5 to 32.5 (Janzen, 1981) results from collecting bias caused by the location of large museums and not an actual biological trend. Further standardized studies must be conducted to record the parasitoid diversity in the Georgia piedmont and surrounding areas. Canada's drop may be easy to explain with its cold climate, and it may still be recovering from the last glaciation. Reasons for the drop in the coastal plain are unclear, but possibly a result of climate or resource fragmentation as we have discussed. One puzzling outcome of this study was that we collected more ichneumonines from San Felasco than in Hitchiti. According to all predictions of decreasing species richness along a gradient, this seems improbable. There were a preponderance of singletons at San Felasco, with 26 (53%) of the 49 ichneumonine species collected only once. However, we cannot explain why there were so many transient individuals at the San Felasco Hammock. Our study may be faulted for only presenting one year of trapping data. However, we believe the data set is sufficient to show the latitudinal trend observed, although, it may not accurately predict total species richness at a given site.
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