The role of climate variability and global warming in the dieback of Northern Hardwoods

The severity of dieback in Northern Hardwood Forests of Canada and the United States this century (1910–1990) was reconstructed from pathology records and compared to indices of extreme weather stresses in the region, and to changes in global temperatures and climatic variability over the same period. Thaw-freeze and root-freeze events in winter and early spring were key factors intriggering (and synchronizing) severe episodes of dieback. Once trees were injured by freezing, forest dieback correlated significantly with heat and drought stress. Freezing (but not drought) stresses in Northern Hardwoods correlated significantly (r = 0.70, p < 0.001) with increasing global mean annual temperatures and low values of the Pacific tropical Southern Oscillation Index. Major diebacks did not occur early in the century at a time of notable freezing stress. Prior to 1940, the Northern Hardwoods consisted of relatively young populations of trees regrowing following extensive cutting and forest burning in the late 19th century (1860–1890). It appears that forest maturation is the key factorpreconditioning trees to climatic injury, and dieback. A simple projection of climate and forest maturation ages suggested the recurrence of major dieback episodes on white/yellow birch, sugar maple and red spruce in the latter half of the 21st century (2045–2085).     

Extreme climatic fluctuations as a cause of forest dieback in the pacific rim

An overview of forest diebacks in regions of the Pacific Rim strongly implicated extreme climatic fluctuations as a cause of dieback in the absence of significant acidic deposition and O₃ pollution. There was strong circumstantial evidence that extreme moisture fluctuations had incited cavitation injury on Eucalyptus, Metrosideros and Nothofagus species with recent dieback. The onset and intensification of crown dieback on Metrosideros in Hawaii related directly to the incidence of extreme rainfall followed by prolonged (2 to 4 weeks) clear, hot, dry weather. Research needs to substantiate the role of an irreversible cavitation dysfunction of the xylem as a mechanism of persistent crown dieback were discussed.     

Principal Forest Dieback Episodes in Northern Hardwoods: Development of Numeric Indices of Areal Extent and Severity

The incidence of forest dieback in the Northern Hardwoods biome of Canada and the United States was determined for period from 1910 to 1990. Information from annual forest service pathology inventories in the two countries and other published literature was coded to estimate yearly the severity and areal extent of dieback on white/yellow birch and sugar maple from 1910 to 1990. Principal dieback episodes occurred as distinct waves coincident with maturation of the forest population in each of six regions. These episodes endured an average of 11 years. It is hypothesized that, once forest populations are mature, they are susceptible to extreme stresses such as freezing and drought which serve to synchronize the onset and subsidence of major dieback episodes.     

Vegetation redistribution: A possible biosphere source of CO2 during climatic change

A new biogeographic model, MAPSS, predicts changes in vegetation leaf area index (LAI), site water balance and run off, as well as changes in Biome boundaries. Potential scenarios of equilibrium vegetation redistribution under 2 × CO₂ climate from five different General Circulation Models (GCMs) are presented. In general, large spatial shifts in temperate and boreal vegetation are predicted under the different scenarios; while, tropical vegetation boundaries are predicted (with one exception) to experience minor distribution contractions. Maps of predicted changes in forest LAI imply drought-induced losses of biomass over most forested regions, even in the tropics. Regional patterns of forest decline and dieback are surprisingly consistent among the five GCM scenarios, given the general lack of consistency in predicted changes in regional precipitation patterns. Two factors contribute to the consistency among the GCMs of the regional ecological impacts of climatic change: 1) regional, temperature-induced increases in potential evapotranspiration (PET) tend to more than offset regional increases in precipitation; and, 2) the unchanging background interplay between the general circulation and the continental margins and mountain ranges produces a fairly stable pattern of regionally specific sensitivity to climatic change. Two areas exhibiting among the greatest sensitivity to drought-induced forest decline are eastern North America and eastern Europe to western Russia. Drought-induced vegetation decline (losses of LAI), predicted under all GCM scenarios, will release CO₂ to the atmosphere; while, expansion of forests at high latitudes will sequester CO₂. The imbalance in these two rate processes could produce a large, transient pulse of CO₂ to the atmosphere.     

Genetic Differences of Pinus Ponderosa [Dougl. Ex Laws.] Trees Tolerant and Sensitive to Ozone

Pinus ponderosa Dougl. ex Laws. one of the most sensitive conifers in western North America to tropospheric ozone, and as such, serves as a model for ozone-phytotoxic effects in forest species. In this paper, we demonstrate differences in level of genetic variation and frequencies of some alleles and genotypes between individuals tolerant and sensitive to oxidant exposure. The degree of sensitivity or tolerance was quantitatively describedusing morphological attributes. Mean value of heterozygosity (Ho) and genotypic polymorphism index (Pg) was statistically significantly higher (p≤ 0.05) in tolerant group of trees, on average 32% for (Ho) and 25% for (Pg). The greatest differences in heterozygosity were found at the Got-A, Got-B, and Shdh loci. More individuals with higher number of heterozygotic loci were noted in tolerant group of trees.     

Three decades of urbanization: Estimating the impact of land-cover change on stream salamander populations

Urbanization has become the dominant form of landscape disturbance in parts of the United States. Small streams in the Piedmont region of the eastern United States support high densities of salamanders and are often the first habitats to be affected by landscape-altering factors such as urbanization. We used US Geological Survey land cover data from 1972 to 2000 and a relation between stream salamanders and land cover, established from recent research, to estimate the impact of contemporary land-cover change on the abundance of stream salamanders near Davidson, North Carolina, a Piedmont locale that has experienced rapid urbanization during this time. Our analysis indicates that southern two-lined salamander (Eurycea cirrigera) populations have decreased from 32% to 44% while northern dusky salamanders (Desmognathus fuscus) have decreased from 21% to 30% over the last three decades. Our results suggest that the widespread conversion of forest to urban land in small catchments has likely resulted in a substantial decline of populations of stream salamanders and could have serious effects on stream ecosystems.     

Acidic deposition: What is fact,what is speculation,what is needed?

In this presentation research findings from the symposium and from the literature are utilized to examine some of the major hypotheses that link acidic deposition with impairment of forest health and productivity in central Europe and eastern North America. Although unequivocal evidence of acid rain damage may be lacking, there is a considerable body of knowledge that implicates air pollutants in recent interference with forest nutrition and health. The nature of the evidence and the inferences that can be drawn from it are still being vigorously debated. The problem of verifying the mechanisms by which air pollutants affect forests still remains. Reports that climatic irregularities have acted as inciting or triggering factors in forest declines are relevant to understanding regional damage. More emphasis on experimental studies that assess interactions of air pollutants and natural stresses with forests is needed.     

Aluminum toxicity in forests exposed to acidic deposition: The ALBIOS results

The ALBIOS project was conducted to examine the influence of acidic deposition on aluminum transport and toxicity in forested ecosystems of eastern North America and northern Europe. Patterns of aluminum chemistry were evaluated in 14 representative watersheds exposed to different levels of sulfur deposition. Controlled studies with solution and soil culture methods were used to test interspecific differences in aluminum sensitivity for one indicator species (honeylocust - Gleditsia triacanthos L. ) and six commercial tree species (red spruce - Picea rubens Sarg., red oak - Quercus rubra L., sugar maple - Acer saccharum Marsh., American beech - Fagus grandifolia Ehrh., European beech - Fagus sylvatica, and loblolly pine - Pinus Taeda L. ). Overall, red spruce was the tree species whose growth was most sensitive to soluble aluminum, with significant biomass reductions occurring at Al concentrations of approximately 200–250 umol/L. Analyses of soil solutions from the field sites indicated that the conditions for aluminum toxicity for some species exist at some of the study areas. At these watersheds, aluminum toxicity could act as a contributing stress factor affecting forest growth.     

Homonymy, synonymy and hybrid misassignments in butternut (Juglans cinerea) and Japanese walnut (Juglans ailantifolia) nut cultivars

Butternut (Juglans cinerea), a tree native to North America and Japanese walnut (J. ailantifolia), native to Japan, form the basis for a small but growing specialty nut crop industry in the eastern United States and Canada. Over the last century, Canadian and American nut tree growers, academic plant breeders and nursery owners have clonally propagated cultivars and freely exchanged scion wood, creating the possibility of misidentification. To detect homonymy, synonymy and hybrid misassignments, we used 12 highly polymorphic microsatellites to genotype most of the butternut and Japanese walnut cultivars grown in the United States and Canada. Bayesian clustering and identity analyses revealed high levels of homonymies (genetically different cultivars with the same name) and synonymies (genetically identical cultivars with different names). Over 41% of the butternut cultivars and 45% of the Japanese walnut cultivars tested had homonymies, and a majority of the cultivars in both species also had synonymies. Further, 43 entries (~15%) identified by the contributors as either J. cinerea or J. ailantifolia were interspecific hybrids. Given our results we recommend that any comparative studies on the cultivars of either species or their hybrids include reference genetic fingerprints as a part of the study.     

Effects of immunocontraception on a suburban population of white-tailed deer Odocoileus virginianus

Abundant populations of white-tailed deer (Odocoileus virginianus) in North America have altered the structure of some forest communities and caused serious conflicts with farmers, gardeners, and motorists, encouraging the search for novel techniques to control populations of deer and other wildlife. We administered the porcine zona pellucida (PZP) immunocontraceptive vaccine to female white-tailed deer living on the 233-ha campus of the National Institute of Standards and Technology (NIST) in Gaithersburg, Maryland, USA. Although some tested PZP preparations proved more effective than others, the number of fawns produced per female was significantly lower in treated than untreated females. Following the onset of contraceptive treatments, the population declined by an average of 7.9% per year, and population declines were larger following years when a higher proportion of females was treated. High mortality due largely to deer-vehicle collisions and low population fertility associated with high deer densities facilitated the observed population decline.     

Forest decline and soil nutritional problems in Pacific areas

Soil nutrient stresses have been determined to contribute to stand-level dieback in two Pacific forest biomes, the Hawaiian Metrosideros rain forest and remnants of the eastern Australian Eucalyptus forest. In the Hawaiian dieback, low levels of N limit indigenous forest development early in primary succession on volcanic soils, while later in primary succession, stresses appear to be associated with soil aging, acidification, loss of cations, decreasing levels of P, increases in soluble Al, and, under poor drainage, sharp increases in soluble Fe. These nutrient limitations put a ceiling on stand development and growth and are considered as one of the three causes predisposing stands to dieback. In the rural or New England dieback of eastern Australia, indigenous eucalypts are adapted to ancient soils with very low levels of P, but pasture improvement with clover and fertilization with superphosphate has imposed different stresses on remnant eucalypts in pastures and nearby forest islands. After fertilization, the trees grow faster initially, but their foliage becomes highly nutritious for insects. Other factors also contribute to a build-up of insects as pests, which now threaten the remaining eucalypts. The rural dieback represents an example of how forests with low canopy species diversity, simplified structure, lack of successional species, and which are prone to dieback under natural conditions, can be destroyed by intensification of agricultural development. The paper closes with a summary of generic factors that were found to cause forest dieback under natural conditions and compares these to the anthropogenically superimposed stresses that led to aggravated tree and forest decline in the Australian rural or New England dieback. The suggestion is made that comparative dieback research at the global level will lead to an improved understanding of natural forest dynamics as an aid in interpreting the new stresses. imposed on forests by human activity.     

Role of air pollution in forest decline in Eastern North America

Evidence for and against three general mechanisms by which air pollution stress may cause or contribute to forest decline in eastern North America is examined. These mechanisms are (1) soil acidification, cation nutrient depletion, and subsequent Al toxicity, (2) direct and indirect effects of gaseous pollutants on the physiology and growth of forest trees; and (3) excess nitrogen deposition and subsequent soil acidification or physiological injury. Recent studies have revealed reductions in base saturation in some sites (both polluted and pristine), but the consequences of these changes to forest health and nutrition are not resolved. Aluminum toxicity may contribute to forest decline in red spruce (Picearubens L.) in high-elevation sites, but the data are contradictory. In forested landscapes in which regional decline (reduced tree growth and/or dieback) is reported, O₃ is the only gaseous pollutant documented as a contributing factor in the eastern North America. Whereas this secondary pollutant exhibits a regional distribution and occurs at potentially phytotoxic levels, a linkage between O₃ and forest decline is substantive only for loblolly pine (Pinustaeda Sarg.) in the southeast. Studies in high elevations do not support the hypothesis that O₃ or hydrogen peroxide directly affects the growth of red spruce or fraser fir (Abiesfraseri Poir.).However, preliminary data link chronic-level O₃ exposure with indirect effects, principally changes in drought tolerance in low-elevations (e.g., P. taeda) nd winter hardiness in high elevations (e.g., P. rubens).The emerging data on the role of air pollution as an environmental stress indicate that indirect effects (i.e., responses in which pollution alters the plant's ability to compete for limited resources or withstand other environmental stresses) are more important than direct effects (e.g., foliar necrotic lesions). Nitrogen saturation has been offered as an hypothesis for P. rubens decline, but no experimental data exist supporting this hypothesis.     

The global distribution of wild tarragon (<Emphasis Type="Italic">Artemisia dracunculus</Emphasis> L.; Asteraceae) cytotypes with twenty-seven new records from North America

Artemisia dracunculus (wild or Russian tarragon), is a polymorphic, herbaceous perennial with a widespread distribution that spans western North America, Eastern Europe and most temperate of Asia. This wild relative of the culinary herb French tarragon has recently been the focus of a number of studies which have investigated its medicinal activity in type 2 diabetes bioassays. The species is documented as having from diploid to decaploid cytotypes and chemical variation has previously been shown to occur between cytotypes. To help focus germplasm collecting efforts for ongoing studies on variation of medicinal compounds within the species, a literature review of the geographical occurrences of cytotypes was conducted. This review revealed a lack of records from North America. In order to fill in this gap in the cytogeographic distribution, meiotic chromosome counts and flow cytometry were used to determine the ploidy level of 27 individuals from 16 different populations throughout the western United States. The results revealed distinct patterns of cytotype distribution. Both diploids and polyploid cytotypes were found in Eurasia, and the distributional range of each cytotype was found to be increasingly restricted as ploidy increased. For North America, even with the inclusion of many new records, only diploid populations were documented, with the exception of one hexaploid record from Arizona which was found in the literature.     

Forest decline and soil nutritional problems in pacific areas

Soil nutrient stresses have been determined to contribute to stand-level dieback in two Pacific forest biomes, the HawaiianMetrosideros rain forest and remnants of the eastern AustralianEucalyptus forest. In the Hawaiian dieback, low levels of N limit indigenous forest development early in primary succession on volcanic soils, while later in primary succession, stresses appear to be associated with soil aging, acidification, loss of cations, decreasing levels of P, increases in soluble Al, and, under poor drainage, sharp increases in soluble Fe. These nutrient limitations put a ceiling on stand development and growth and are considered as one of the three causes predisposing stands to dieback. In the rural or New England dieback of eastern Australia, indigenous eucalypts are adapted to ancient soils with very low levels of P, but pasture improvement with clover and fertilization with superphosphate has imposed different stresses on remnant eucalypts in pastures and nearby forest islands. After fertilization, the trees grow faster initially, but their foliage becomes highly nutritious for insects. Other factors also contribute to a build-up of insects as pests, which now threaten the remaining eucalypts. The rural dieback represents an example of how forests with low canopy species diversity, simplified structure, lack of successional species, and which are prone to dieback under natural conditions, can be destroyed by intensification of agricultural development. The paper closes with a summary of generic factors that were found to cause forest dieback under natural conditions and compares these to the anthropogenically superimposed stresses that led to aggravated tree and forest decline in the Australian rural or New England dieback. The suggestion is made that comparative dieback research at the global level will lead to an improved understanding of natural forest dynamics as an aid in interpreting the new stresses imposed on forests by human activity.     

Changes of lignin phenols and neutral sugars in different soil types of a high-elevation forest ecosystem 25 years after forest dieback

Long-term effects of forest disturbance 25 yr ago on lignin and non-cellulosic polysaccharide pools in an unmanaged high-elevation Norway spruce (Picea abies L. [Karst.]) forest were investigated by comparing three dieback sites with three adjacent control sites with non-infested spruce on identical soils. Samples were taken from the forest floor and the mineral soil; one Ah horizon sample per site was physically fractionated into density and particle size fractions. Additionally, changes in the above- and belowground input of lignin and non-cellulosic polysaccharides after forest dieback were quantified. Lignin and its degree of structural alteration in plant and soil samples were assessed by CuO oxidation and subsequent analysis of the lignin phenols. Non-cellulosic polysaccharides were determined after hydrolysis with trifluoroacetic acid (TFA), derivatisation of their neutral sugar monomers by reduction to alditols, and subsequent acetylation. The total plant-derived input of lignin and non-cellulosic polysaccharides to the soil was similar for the dieback and the control sites. The chemical composition of the input has changed considerably after forest dieback, as shown by significantly higher syringyl/vanillyl (S/V) ratios and significantly lower (galactose+mannose)/(arabinose+xylose) (GM/AX) ratios. This indicates a changed plant input and a higher contribution of microbial sugars. Contents of lignin phenols in the forest floor and coarse particle size fractions of the A horizons were significantly smaller at the dieback sites (p<0.01). Moreover, larger acid-to-aldehyde ratios of vanillyl units (Ac/Al)_v indicated an increased degree of lignin phenol alteration. Also contents of neutral sugars were significantly (p<0.01) smaller in the forest floor, but not in the A horizons of the dieback sites. The GM/AX mass ratios as well as the (rhamnose+fucose)/(arabinose+xylose) (RF/AX) ratios in the forest floor and coarse particle size fractions of the mineral topsoil were significantly (p<0.01) larger after forest dieback, indicating a larger relative contribution of microbial sugars. In general, the lignin phenol and neutral sugar pools of all three soil types exhibited similar response patterns to the changed site conditions. Our results demonstrate that the lignin and neutral sugar pools of humic topsoil horizons are highly sensitive to forest disturbances. However, the two compounds show different patterns in the mineral soil, with the major neutral sugar pool being stabilized against changes whereas the lignin phenol pool decreases significantly.     

Characterization of American hazelnut (Corylus americana) accessions and Corylus americana?×?Corylus avellana hybrids using microsatellite markers

The American hazelnut (Corylus americana Marshall) is native to the eastern United States and Southern Canada. In the early decades of the last century, breeding work by several individuals attempted to combine the cold hardiness and disease resistance of the American hazelnut with the larger nut size of the European hazelnut (C. avellana L.). Many hybrid selections grown today trace back to these early efforts. Over the past three decades, representatives of C. americana were collected and are preserved in Corvallis, Oregon. Seeds were collected along roadsides, in hedgerows, in woodland clearings, and in gardens. The seeds were germinated and the best of the resulting seedlings were preserved for later use. In this study, genetic diversity was studied in 87 American and 67 hybrid hazelnut selections using 21 microsatellite loci. The total number of alleles was 266 in the 162 accessions examined, of which 229 were present in C. americana accessions, but only 168 in the Arbor Day Farm hybrids, and 116 in the hybrids of C. americana ‘Rush’. In the American accessions, a high level of genetic diversity was observed (H _e ?=?0.74, H _o ?=?0.68). A genetic similarity matrix of the American and hybrid accessions, and a few European cultivars, was constructed and the resulting dendrogram revealed seven major groups: European cultivars and ‘Rush’ hybrids, two groups of Arbor Day Farm hybrids, three groups of C. americana accessions, and a mixed group of hybrid and American accessions. Analysis confirmed the reported parentage of 10 hybrids. The genetic diversity among the American hazelnut accessions, untapped to date, will be useful in breeding hybrids that will allow expansion of hazelnut production into eastern North America.     

Status of the Pelecanidae

The recent history, current status and prospects in the immediate future of the seven species of the Pelecanidae are reviewed. As a consequence of pesticide poisoning, Pelecanus occidentalis suffered severe population declines in the 1950s and 1960s in portions of its range in the United States. However, since the ban on use of DDT in 1972 the species is again laying eggs of near normal thickness, reproductive success appears to be normal and populations are stable or increasing. Similarly, available data indicate that the world populations of P. rufescens, P. conspicillatus, and P. erythrorynchos remain stable, although local population fluctuations do occur. Data for P. onocrotalus show a stable population in Africa but a decline in Asia and Europe, both in numbers of birds and breeding colonies. More seriously, only very small populations of P. crispus and P. philippensis exist. Fewer than 1000 pairs of P. crispus next in 19 colonies in eastern Europe and Asia. Fewer than 1200 pairs of P. philippensis nest in four colonies in eastern/southern India and 23 colonies in Sri Lanka. The populations of both species have declined considerably in the past few decades. The causes for the declines are not documented but are thought to result from a combination of human disturbance in nesting colonies; destruction of nesting and roosting-loafing areas; declines in fish availability; and pesticide contamination. Only immediate action and concerted efforts at stabilizing the populations in the wild, in conjunction with the establishment of captive breeding populations, will preserve these two species from extinction.     

Comparison of forest soil carbon dynamics at five sites along a latitudinal gradient

The aim of this study was to compare the turnover time of labile soil carbon (C), in relation to temperature and soil texture, in several forest ecosystems that are representative of large areas of North America. Carbon and nitrogen (N) stocks, and C:N ratios, were measured in the forest floor, mineral soil, and two mineral soil fractions (particulate and mineral-associated organic matter, POM and MOM, respectively) at five AmeriFlux sites along a latitudinal gradient in the eastern United States. Sampling at four sites was replicated over two consecutive years. With one exception, forest floor and mineral soil C stocks increased from warm, southern sites (with fine-textured soils) to cool, northern sites (with more coarse-textured soils). The exception was a northern site, with less than 10% silt-clay content, that had a soil organic C stock similar to the southern sites. A two-compartment model was used to calculate the turnover time of labile soil organic C (MRT_U) and the annual transfer of labile C to stable C (k₂) at each site. Moving from south to north, MRT_U increased from approximately 5 to 14 years. Carbon-13 enrichment factors (ε), that described the rate of change in δ¹³C through the soil profile, were associated with soil C turnover times. Consistent with its role in stabilization of soil organic C, silt-clay content was positively correlated (r = 0.91; P ≤ 0.001) with parameter k₂. Latitudinal differences in the storage and turnover of soil C were related to mean annual temperature (MAT, °C), but soil texture superseded temperature when there was too little silt and clay to stabilize labile soil C and protect it from decomposition. Each site had a relatively high proportion of labile soil C (nearly 50% to a depth of 20 cm). Depending on unknown temperature sensitivities, large labile pools of forest soil C are at risk of decomposition in a warming climate, and losses could be disproportionately higher from coarse textured forest soils.     

Decline of bumble bees (Bombus) in the North American Midwest

Declines in many bumble bee species have been documented in Europe raising several ecological and economic concerns. The nature and extent of bumble bee decline in North America is poorly understood due mainly to a lack of baseline and long-term data. Museum collections provide excellent sources of information on past and current species distributions, which can be used to infer changes in the composition of insect communities. Using the Illinois Natural History Survey’s electronic database of Hymenoptera and a recent biodiversity survey of historically sampled localities, we were able to examine changes in the richness and distribution of the bumble bee fauna of Illinois over the last century. We found that bumble bee species richness declined substantially during the middle of the century (1940-1960). Four species were locally extirpated: Bombus borealis, Bombus ternarius, Bombus terricola and Bombus variabilis. The ranges of Bombus affinis, Bombus fraternus, Bombus pensylvanicus and Bombus vagans have also decreased in Illinois. Our analyses also indicated that current bumble bee diversity is highest in northern Illinois, where conservation efforts would be most productive. Our study demonstrates that half of the bumble bee species found historically in Illinois have been locally extirpated or have suffered declines, supporting observations of broader declines in North America. Major declines in the bumble bee fauna coincided with large-scale agricultural intensification in Illinois between 1940 and 1960. Attempts to conserve bumble bees in Illinois should involve wildlife-friendly approaches to agriculture, such as increasing agricultural land set-asides and hedgerows, and employing integrated pest management.     

Effects of simulated acidic rain on one species each ofpseudoparmelia,usnea, andumbilicaria

The lichensPseudoparmelia caperata (L.) Hale,Usnea ofsubfusca Stirt., andUmbilicaria mammulata (Ach.) Tuck. were exposed to simulated acidic rain with pH levels of 2.3, 3.0, 3.3, 4.3, or 5.6 and other. ions in concentrations normally found in rain in the eastern United States. The pH levels of the most acidic treatments (3.3, 3.0, 2.3) were similar to those found in fog, cloud water, and occasional rainfall events. The pH 4.3 and 5.6 treatments compared to average ambient conditions in the eastern and western United States, respectively, and caused no significant effects on photosynthesis. However, after the first week of treatment, significant effects of rain pH at the most acidic treatments on gross photysnthesis were detected inP. caperata andU. mammulata, but not inU. cfsubfusca. Visible effects of injury were also observed and included bleaching, necrotic spots, and necrotic margins, which resembled damage seen in field populations ofU. mammulata, the most sensitive species.