EXAMPLE OUTLINE - EASTERN DECIDUOUS FOREST

Eastern deciduous forest (USA)

Focal species: oaks, maples, deer, gypsy moth, mice, ticks, Lyme disease (spirochete), songbirds, earthworms, mycorrhizae, ants

Key topics: plant-herbivore interactions (seed predation, masting, plant defense), prey-predator interactions (gypsy moth pupae-mice, and insect herbivores-songbirds), host-parasite interactions (mice/deer/humans-ticks, and gypsy moth-virus), mutualisms (mycorrhizae, ant-seed, frugivore), population dynamics, episodic events, eastern deciduous forest in North America, glaciation, forest fragmentation, new diseases, nutrient cycling, nitrogen cycle

Human interest: glaciation, gypsy moth, Lyme disease, extinction of dominant species, global warming, acid rain

Nuts ¹

• Nut-producing tree species evolved traits that facilitate nut (seed embryo plus food) dispersal by certain rodents and corvids while reducing nut predation by others
• Large nutrient reserve attracts dispersers and facilitates quick establishment with large photosynthetic surface and extensive roots; counters major mortality factors – drought, insufficient on forest floor, browsing by herbivores, competition with plants
• Acorns contain tannins, tannins can bind with nutrients (preventing assimilation across gut wall of seed predator) and have toxic effects (on cells of gut lining)
• Acorns of “black oak” group (includes red oaks) have higher tannin levels than “white oak” group
• White oak acorns germinate in fall of production, whereas others germinate after overwintering
• Consumers (e.g., squirrels, grackles, blue jays) usually only eat cap-end of acorn which has less tannins, plant embryo is in other end so germination still possible ²
• Rodents disperse nuts up to 100 m ¹
• Some consumers bury acorns, if scatter hoarders and not retrieved later, then “planting” them, usually in favorable germination sites
• Most nuts lack long-term dormancy, e.g., white oak acorns have no dormancy, and so germinate within days of maturing in fall
• Dispersers exhibit (morphological and behavioral) adaptations , e.g., gray squirrels often excise embryo of white oak acorn before burial but don’t do that with red oak acorns which overwinter as acorns

Masting ^3,4

• Many oak species produce a large seed (acorn) crop every 2-6 years, with low or no production in between
• Masting reflects internal interaction of carbon storage and allocation patterns to growth versus reproduction in oaks, with weather influencing time between masting
• Masting may be advantageous by satiating seed predators and thus some seeds survive
• Most advantageous if masting occurs in years when other nut-producing species are not masting
• Some other major consumers: white-footed mice, eastern chipmunks, white-tailed deer
• These three are also major hosts for deer ticks
• Mice also important predators of other tree seeds (maple) and gypsy moth pupae
• Deer also browse understory woody and herbaceous plants
• Deer browsing and gypsy moth defoliation of trees reduces songbird abundance
• Masting (in fall) correlated to increased mouse density (following summer)
• High mouse density correlated to high predation on gypsy moth pupae
• Mast crop failure (in fall) correlated to low mouse density and low gypsy moth pupal predation following summer
• High acorn density correlated to attracting deer, resulting in high density of ticks

Gypsy moth ^3,4

• Gypsy moth (Lymantria dispar) is native to Europe and Asia, not as much problem there
• Deliberately brought to USA (by French artist in late 1860s) for purpose of developing a silk producer by hybridizing with native moths
• Accidentally escaped, spread through New England, now throughout northeastern USA
• Prefer oak leaves but will eat leaves of many other woody species, mainly older larvae that utilize other woody species
• Gypsy moth larvae have an elevated midgut pH which would dissociate leaf protein from leaf tannins (complexes formed under acid conditions of macerating leaf tissue which is fairly acid (23 tree species with pH ranging from 4.0 to 6.2) and well buffered (resistant to change) ⁵
  • Energetic cost to maintaining alkaline gut taking in acidic leaf material
  • Older larvae have more alkaline midgut so can exploit wider range of tree species
  • Alkaline midgut also facilitates surfactant properties of ingested lipids so increases uptake and inhibit tannin-protein binding
  • Alkaline midgut facilitates epoxidase activity, which detoxifies terpene-derived toxins
  • Also, infecting stage of NP virus and toxin of Bacillus thuringiensis (bacteria used as biocontrol) require alkaline conditions, so cost to gypsy moth larvae of having alkaline gut
• Egg masses overwinter, hatch in spring, larvae move to top of trees, spin down on silk threads and disperse by wind, larvae eat leaves, pupate in early summer, adults mate in summer, females flightless, attract males with pheromone & lay one large batch of eggs
• Population peaks about every 9-10 years, outbreak levels result in wide-spread defoliation, which can affect masting cycle, weaken or kill trees, and increase competition among woody species for resources (by increasing light to understory woody species)
• Decline from peak population levels reflects limited food quantity, effects of poor food quality (increased plant defenses), mortality due to parasitoids, viral and fungal pathogens, and predation by mice
• Feeding affects foliage quality (tannins increase) but changes don’t seem to drive population cycles ⁶
• Nuclear Polyhedrosis virus (NPV) – most insect species not affected, high concentration of tannins can inhibit NPV which may contribute to variation in outbreak patterns, yet at high population density of gypsy moths largest and most important source of mortality, often causes collapse of population
• Fungus Entomophaga maimaiga – accidentally introduced, some other insects may be affected
• Parasitoid rates generally relatively low
• Weather patterns weakly correlated with population patterns, indirect effect by contributing to masting pattern, direct effect if very cold winter or cool spring
• European version in North America - female does not fly so dispersal reduced, but hybridizes with Asian version (accidentally introduced in early 1990s) which does fly
• “Temporal and spatial patterns of mast production may be responsible for the episodic and spatially synchronous behavior of gypsy moth outbreaks in North America.” ⁶
  • Density-dependent mortality limits high-density populations
  • Little evidence for strong regulation at low density, small mammals major source of mortality but generalists and not prefer gypsy moths, predation levels reflect small mammal abundance, which is linked to masting patterns and lags masting pattern
  • Masting has considerable spatial synchrony over large geographic areas, thus gypy moth outbreak over large geographic areas reflects masting effect on small mammals abundance
  • “This multitrophic relationship among mast, predators, and gypsy moths represents a very different explanation of forest insect outbreak dynamics than the more widely applied theories based upon predator-prey cycles or feedback with host foliage quality.” ⁶

Lyme disease ^3,4,5

• Lyme disease was named in 1977 when arthritis (joint aches) was observed in a number of children in the area of Lyme, CT
• Symptoms: “bull’s-eye” erythema, and non-specifics such as fever, fatigue, headache, muscle and joint aches ⁸
• Lyme disease caused by spirochete (Borrelia burgdorferi), transmitted by bite of tick vector (Ixodes sp.)
• Ticks have 4 stages: egg, larva, nymph and adult; larva, nymph and adult each take one blood meal, then drop off host, larva and nymph molt then find new host, adults mate on host; so 4 stages, 3 blood meals, 2 years for life cycle from egg to adult
• Immature ticks normally feed on small vertebrates (birds, mice, lizards) and adult ticks on deer
• Many ticks never infected because many host species not efficient for transmission, most “competent” transmission is in white-footed mice (40-80% transmission), so white-footed mice are major reservoir
• Female tick reproduces once & dies, spirochete rarely transmitted from mother to eggs, thus transmission only from “reservoir host” to immature tick (and not vice versa)
• Adult ticks feed on deer, deer attracted to acorn-rich oak areas, adult ticks mate on deer & drop off there overwintering & females deposit eggs there; eggs hatch in spring, larvae feed on birds and small mammals and molt to nymph in late summer, overwinter then feed following spring/summer, humans most likely infected by nymphs (1mm in size), so Lyme disease shows up in humans in late spring-summer (1-2 week incubation), nymphs molt to adult, adults feed on deer and mate and drop off in fall
• Correlation between number of acorns and number potentially infected tick nymphs: 2-year lag; masting attracts deer, lots of tick eggs deposited to those sites, mice population increases there (overwinter better due to masting), ticks have abundant supply of mice hosts, mice best spirochete reservoir, 2nd summer after mast will be high risk time and place (high density tick nymphs having fed on mice) for Lyme disease
• Areas in eastern USA where residential area adjacent to forest increasing dramatically
• Population density of white-footed deer mice and deer is high in forest fragments, predator populations in general reduced by humans ⁷
• Lyme disease risk is 10x greater in small forest fragments than larger fragments, small forest fragments near human dwellings and activity

Past and future forest

• Dramatic changes since glaciation; dramatic changes predicted with global warming
  • About 20,000 years ago, ice or tundra where northeastern US forests are now ⁹
  • Forest tree species are still migrating into previously deglaciated areas, average interglacial period too short for floristic equilibrium to be obtained
  • Selection through Pleistocene produced species successful in invading communities, deciduous trees and hemlock migrate relatively rapidly
  • About 16,000 years ago (peak of last glaciation), nut-producing trees (oaks, beech, hickories) restricted to southeastern US ¹
  • Reached northern edge of current ranges between 10,000 and 12,000 years ago; recolonization rate varied with species, but as fast or faster than wind-dispersed tree species (maples, firs, hemlock, spruces)
  • Food-caching rodents and jays had major role as seed dispersers
  • Once nearly continuous forest now fragmented by agricultural, superhighways, cities and suburbs
  • With global warming, deciduous forest should expand northward, but concern about colonization rate due to fragmentation limiting dispersal agents?
• Composition of eastern deciduous forest was different prior to colonization of North America by Europeans ¹⁰
  • White oak rather than red oak was a dominant then
  • White oak acorns germinate in fall, red oak acorns don’t germinate until spring
  • Huge numbers of passenger pigeons (3-5 billion, equal to current number of birds of all species overwintering in USA), hunted to extinction by late 1800s
  • Major acorn eaters especially in spring when nesting, probably to detriment of red oak
• Composition continues to change
  • Red maple now dominates understory of many oak, pine and northern-hardwood forests, and so increase in overstory dominance during this century ¹¹
    • Low resource requirements and “supergeneralist” so characteristics of both early and late successional species
    • Thrives in many landscapes, different soil conditions and light regimes
    • Benefits from fire suppression, oaks would benefit if fire frequent
    • High populations of seed-eating and sapling-browsing deer probably hurt oak more than maple, which have alkaloids as chemical defense
    • Seeds germinate soon after production in spring, early reproductive maturity at 4-10 years, maximum longevity ~200 years
• Other introduced insect herbivores to North American forests, NA forests susceptible to introduced species but why? ¹³
  • That Europe and North America once joined predisposes them to successful interchange of insect herbivores, but why have European insects been 100x more successful at invasion into North America than vice versa?
  • Number of successful invaders determined by ecological opportunities upon arrival
    • Potential host plant species (taxonomically or chemically related), and their abundance, morphological, ecological and phenological similarity to native hosts
    • In NA larger number of potential host plants (north of 35o, 2x more tree species due to less extinction during glaciation due to north-south mountains rather than east-west as in Europe), greater abundance (tree abundance 2x greater), less fragmented distribution than in Europe (with longer and intense disturbance by humans)
    • Abundant alien plants from Europe (30-60% during early succession in NA) facilitates establishment by European insects
  • Invaders are intrinsically competitively superior than natives
    • Since Alps developed, European biota more severely impacted than any other by cyclical severe climate changes driven by Earth’s orbital fluctuations (e.g., glaciation from north and glaciers in east-west mountains left little refuge for plants and animals, and created aridity in southern Europe
    • Since last 10,000 years humans with invention of agriculture disrupted and even wholly eliminated many ecosystems in Europe
    • Selects for suite of traits that facilitate survival in patchy, fragmented, impoverished forests: high behavioral, morphological and physiological plasticity; uniparental reproduction (parthenogenesis) (40% of introduced insects on woody plants compared to 11% native insects), large reproductive potential, auto- and alloploidy, strong dispersal capability, efficacy in dealing with competitiors, predators and parasites, special stress tolerance such as extended dormancy
    • Rapid and perfect synchronization of invader’s life cycle to that of new environment and hosts, insects coming from 50o to 40o latitude (northern Europe to New England) no problem, but other direction is problem because summer day length in northern Europe too long to trigger diapause for a New England adapted insect
  • Risk of continued immigration of insect species into NA is high
• Forest songbirds
  • Effects on community
    • Birds learn how to find insect prey among tree species ¹⁴
    • Birds reduce densities of leaf-eating insect herbivores in forests ¹⁵
    • Birds by eating leaf-feeding insect herbivores increase growth of trees ¹⁶
  • North American songbirds declining: various hypotheses ¹⁷
    • Size of forests (fragmentation, small plots, fewer species)
    • Edge effect (forest margins different habitat)
    • Migrating birds less likely to find small plots
    • Tropical deforestation affect migrants (overwinter in tropics but nest in North America)
    • Long-distance migrants more vulnerable (arrive later on breeding sites, narrower window, disturbance bigger impact)
    • Nest predators increasing in fragmented forests which are in suburban areas, very strong evidence for this
    • Nest parasites such as brown-headed cowbird increasing, very strong evidence for this
    • Fragmented areas becoming population sinks and sources more problematic

Mutualisms

• Mycorrhizae
  • Roots of most plants involved in symbiosis with mycorrhizal fungi, fungi function as root hairs penetrating soil, facilitate uptake of phosphorus and other nutrients, plant supplies carbohydrates to fungus
  • Endomycorrhizae (hyphae penetrate outer cells of plant root) and ectomycorrhiae (hyphae surround but do not penetrate roots), probably played role in colonization of land by early land plants
  • Ecto-type characteristic of trees and shrubs especially in temperate regions, so pines, firs, oaks, beeches and willows; symbiosis may facilitate resistance to harsh conditions or be facilitated by plant species with more resistance
• Ants and seeds ¹⁸
  • Eastern deciduous forest typically means relatively nutrient poor soil, seeds are the dispersal stage, some plants have evolved traits that facilitate getting seeds to favorable germination sites
  • Some herbaceous perennials and shrubs produce seeds with external tissue (elaiosome) that is rich in fats or protein and contain chemical attractants, e.g. some violets
  • Ants carry seeds to colony, chew off external tissue, may store seed or discard on trash pile (seed coat very hard but ant mandibles scarify which helps seed absorb moisture), other refuse in trash pile makes it nutrient rich, ant mounds due to excavations have aerated soil and water retention
  • Experiments show that seeds with elaisome usually deposited unharmed, trash piles nutrient rich, seeds have higher germination there, better survivorship and more reproduction
• Frugivory ¹⁹
  • In eastern deciduous forest, 125+ species of woody tree, shrubs and vines that produce fruits, with seeds dispersed primarily by birds
  • Fruit quality patterns: 1) summer small seeds - low lipids, high sugars, low retention on plant; 2) summer large seeded – low lipids, variable sugar amount, low retention; 3) fall high quality – large seeds, high lipids, variable sugar, variable retention; 4) fall low quality – variable seed size, low lipids, low sugar, high retention = “long shelf life”
  • Many bird species in eastern deciduous forest eat fruits, for some it is a major part of diet for some of the year, major species are thrushes and waxwings
  • Fruit ripening patterns: 1) summer fruits tend to exhibit 3 color stages, “immature” green then to “intermediate color” then “ripe” color, e.g. green to pink/red to blue/black, as in blueberries or blackberries and cherries, that may signal territorial birds and thus increase dispersal by “quality dispersers” as opposed to small mammals, and 2) fall fruits may have early foliage color change that may signal migratory birds, or overwinter retention of fruits thus dispersal by overwintering birds
  • Different seed dispersers likely to generate different seed shadows

Nutrient cycling

• Soil is produced by weathering of bedrock (rock consisting of a variety of minerals (elements combined into inorganic compounds)), soil production is facilitated by organic acids from plant matter, mineral content combined with organic matter via weathering and biotic processes (action of microbes and soil invertebrates), layering reflects which processes dominant from surface through soil to bedrock
• Quality and quantity of soil is patchy across forest floor, pit-and-mounds contribute to patchiness, affects distribution of understory plants ²⁰
• Hubbard Brook experiment, which can be found in almost every ecology textbook
• Acid rain
  • Sulfuric acid is main acid (50-75%) that develops from industrial emissions (especially power plants using fossil fuel), records from 1963 into 1990s show precipitation in northeastern US with average pH of 4, Europe with similar problem
  • Calcium
    • Natural source is from weathering of bedrock
    • Calcium important in cambial growth of trees and sapwood functioning which affects crown density (leaf mass and area, too)
    • Acid rain resulted in loss of 50% calcium over 45 years at Hubbard Brook EF
    • Without enough calcium (and magnesium) to neutralize acid rain aluminum ions released into soil, aluminum ions reduce uptake of calcium by plants (competition for binding sites on fine roots), also aluminum toxic to plants, overall makes plants more vulnerable to diseases and insects ²¹
    • In Europe forest birds producing eggshells that are thinner and thus high rate of nesting failure, calcium deficiency, snail shells are main calcium source for birds, but now snails scarce, decrease in calcium on nutrient poor (most forest soils are) acidified soils ²
  • Nitrogen saturation ²³
    • Sulfuric acid deposition from acid rain (due to burning fossil fuels) has been a concern, but now also worried about nitrogen from same source
    • Forest ecosystems usually nitrogen limited, so how can increased nitrogen be a stressor?
    • Accumulates, exceeds capacity of system for uptake, other resources (usually phosphorus and water) rather than nitrogen limit plant growth
    • May result in nitrate leaching to streams and groundwater (which may increase microbial levels
• Fixing acid rain; if acid rain’s effects were direct on trees, lakes and streams then seems simple – just cut industrial emissions especially sulfur, USA 1970 Clean Air Act and 1990 amendments (reducing sulfur emissions to 50% of 1980 level by 2000), has this worked? ²⁴
  • Cut backs in emissions (somewhat), concentration of sulfur in water declined, but water low in acid neutralizing capacity, effect of acid rain still strongly present
  • Thinking at time of legislation was that soils were so well buffered that acid rain didn’t have serious direct effect there
  • But no, acid rain made profound changes in soil, best data set in US is Hubbard Brook Experimental Forest in New Hampshire
  • Acid rain caused leaching of calcium from soil to water, emissions cutback also reduced calcium input, so little to counter loss, will be 50+ years before weathering of bedrock can restore calcium pool
  • Some European countries spread lime in forests, too expensive here
• Earthworms eat dead leaves and so affect soil ¹²
  • Native earthworms are rare in northern forests of North America, presumably wiped out during last glaciation and slow to recolonize
  • Most earthworms in northern forests now are exotic, introduced recently
  • Not known what long term effects that will have, how wide-spread invasion is, what areas are susceptible and how that will change with global warming, how other factors such as acid rain deposition will affect invasion or its effects?
  • Earthworms can eliminate the forest floor (organic layer), which is key component to stability of forests (e.g., protects against erosion, facilitates regeneration after disturbance)
  • Earthworm activity may reduce availability of phosphorus to plants, and stimulate nitrogen cycle processes (and thus loss of fixed nitrogen)
  • Mycorrhizal activity may be less

Eastern deciduous forest: Lyme disease, masting, and gypsy moths
Eastern deciduous forest: Mutualisms and nutrient cycling
Outlines for Eastern deciduous forest material
References for Power of Story examples

¹ Vander Wall SB (2001) The evolutionary ecology of nut dispersal. Botanical Review 67:74-117 [Great resource about patterns and hypotheses.]

² Steele MA, Knowles T, Bridle K, Simms EL (1993) Tannins and partial consumption of acorns: implications for dispersal of oaks by seed predators. American Midland Naturalist 130:229-238

³ Jones CG, Ostfeld RS, Richard MP, Schauber EM, Wolff JO (1998) Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 279:1023-1026 [Removing mice resulted in more moths; adding acorns increased mice density and tick density, with ticks the vector for Lyme disease.]

⁴ Ostfeld RS, Jones CG, Wolff JO (1996) Of mice and mast. BioScience 46:323-330 [Feedback among oaks (acorns), deer (eating foliage and acorns), mice (eating acorns, maple seeds and gypsy moth pupae), and ticks (carried by deer and mice and carriers of Lyme disease) generating episodic events in deciduous forest of eastern US]

⁵ Schultz JC, Lechowicz MJ (1986) Hostplant, larval age, and feeding behavior influence midgut pH in the gypsy moth (Lymantria dispar). Oecologia 71:133-137 [Examines gut physiological adaptations versus leaf chemistry to assess gypsy moth’s ability to be a generalist feeder.]

⁶ Liebhold A, Elkinton J, Williams D, Muzika R (2000) What causes outbreaks of the gypsy moth in North America? Population Ecology 42:257-266 [“Temporal and spatial patterns of mast production may be responsible for the episodic and spatially synchronous behavior of gypsy moth outbreaks in North America. This multitrophic relationship among mast, predators, and gypsy moths represents a very different explanation of forest insect outbreak dynamics than the more widely applied theories based upon predator-prey cycles or feedback with host foliage quality.”] http://www.sandyliebhold.com/pubs/rpe_gm.pdf

⁷ Ostfeld RS, Keesing F (2000) Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14:722-728 [“The reservoir competence of hosts within vertebrate communities and the degree of specialization by ticks on particular hosts will strongly influence the relationship between species diversity and the risk of exposure to the many vector-borne diseases that plague humans.”]

⁸ Koren HS, Crawford-Brown D (2004) A framework for the integration of ecosystem and human health in public policy: two case studies with infectious agents. Environmental Research 95:92-105 [Lyme disease increasing due to rapid suburbanization and reforestation resulting in fragmented forest adjacent to human dwellings. Fragments have high populations of white-footed mice (reservoir for spirochete causing disease) and deer, which in addition to mice host tick vector, but few or no predators to keep mice and deer populations in check.]

⁹ Davis MB (1976) Pleistocene biogeography of temperate deciduous forests. Geoscience and Man 13:13-26 [Good summary]

¹⁰ Ellsworth JW, McComb BC (2003) Potential effects of passenger pigeon flocks on the structure and composition of presettlement forests of eastern North America. Conservation Biology 17:1548-1558 [Suggest widespread and frequent disturbance of forests by huge, roaming flocks of pigeons, via roosting behavior causing limb breakage and thus creating fire fuel, guano deposition killing understory plants and seed-eating favoring fall germinating oaks over spring germinators.]

¹¹ Abrams MD (1998) The red maple paradox. BioScience 48:355-364 [An explanation for the widespread expansion of red maple in eastern forests.]

¹² Hendrix PF, Bohlen PJ (2002) Exotic earthworm invasions in North America: Ecological and policy implications. BioScience 52:801-811; Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC, Suarez E, Pelletier DM, Fahey RT (2004) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1-12 [Summary of a set of research papers in that volume. Too early to have a clear picture of what the outcome of earthworm invasion will be, but large effects are quite likely.]

¹³ Niemela P, Mattson WJ (1996) Invasion of North American forests by European phytophagous insects. BioScience 46:741-753 [“European biota may be much better competitors, especially under disturbance and fragmented conditions, than their North American counterparts.”]

¹⁴ Heinrich B, Collins SL (1983) Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64:592-602; Heinrich B (1979) Foraging strategies of caterpillars: leaf damage and possible predator avaoidance strategies. Oecologia 42:325-337 [Series of observations and experiments that show how caterpillars evade birds, and how birds search for caterpillars and the role of learning.]

¹⁵ Holmes RT, Schultz JC, Nothnagle P (1979) Bird predation on forest insects: an exclosure experiment. Science 206:462-463

¹⁶ Marquis RJ, Whelan CJ (1994) Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology 75:2007-2014

¹⁷ Terborgh J (1992) Why American songbirds are vanishing? Scientific American (May):98-104 [Engaging article that considers various hypotheses, summarizes data, and indicates complexities clearly. Reports since 1992 for USA (and Europe) indicate continuing decline.]

¹⁸ Handel SN, Beattie AJ (1990) Seed dispersal by ants. Scientific American 263 (2/Aug):76+; Beattie AJ (1990) Ant plantation. Natural History Feb:10-14 [Engaging descriptions plus good illustrations and photographs.]

¹⁹ Stiles EW (1980) Patterns of fruit presentation and seed dispersal in bird-disseminated woody plants in the eastern deciduous forest. American Naturalist 116:670-688; Stiles EW (1984) Fruit for all seasons. Natural History October: 43-52 [Data amassed in first article; engaging description and photographs in second.]

²⁰ Beatty SW (1984) Influence of microtopography and canopy species on spatial patterns of forest understory plants. Ecology 65:1406-1419

²¹ Shortle WC, Smith KT (1988) Aluminum-induced calcium deficiency syndrome in declining red spruce. Science 240:1017-1018

²² Graveland J, van der Wal R, van Balen JH, van Noordwijk AJ (1994) Poor reproduction in forest passerines from decline of snail abundance on acidified soils. Nature 368:446-448

²³ Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. BioScience 39:378-386 [“Excess nitrogen from fossil fuel combustion may stress the biosphere.”]

²⁴ Likens GE, Driscoll CT, Buso DC (1996) Long-term effects of acid rain: response and recovery of a forest ecosystem. Science 272:244-247

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