422 Northeastern Naturalist Vol. 16, Special Issue 5
Biology of Ultramafic Rocks and Soils:
Research Goals for the Future
Robert S. Boyd1,*, Arthur R. Kruckeberg2, and Nishanta Rajakaruna3
Introduction
At this, the 6th International Conference on Serpentine Ecology, it seems
timely to review briefly the present status of the field and to project the
needs for future research. Although a great deal of serpentine research was
done prior to 1960, as summarized by Krause (1958) and discussed briefly
by Brooks (1987), much of our progress in learning how serpentine geology
affects plant and animal life occurred in the mid- to late 20th century. In that
era, it was the landmark studies of several scientists worldwide that initiated
a meteoric increase in published serpentine research. Key players in setting
the stage for this burgeoning output included pioneers in Europe (e.g., John
Proctor, Stan Woodell, Ornella Vergnano, and Olof Rune), North America
(e.g., Herbert Mason, Robert Whittaker, Hans Jenny, Richard Walker, and
Arthur Kruckeberg); and elsewhere (e.g., Robert Brooks, Alan Baker, Roger
Reeves, and Tanguy Jaffré). All made notable contributions to understanding
the “serpentine syndrome.”
Despite the flourishing of serpentine studies in recent years, there is
much “unfinished business.” After all, an axiom of science is that there
is an unending quest for answers. In the many subdisciplines of geology
and the soil and plant sciences, serpentine areas still hold mysteries—
unsolved questions and challenges for the future. We now examine some
of them, organized by the five major topic areas covered by the conference
(Geology and Soils, Biota, Ecology and Evolution, Physiology and Genetics,
and Applied Ecology), and point out how some of the contributions at
the conference, and some that are included in this Proceedings Special Issue,
address them.
Geology and Soils
Biologists loosely use the term “serpentine” to describe rocks that are referred
to by geologists as “ultramafics.” Interpretation of ultramafic geology
underwent major changes in the late 20th century. Before the plate tectonics
revolution, ultramafics were baffling and often controversial lithological
1Department of Biological Sciences, 101 Life Sciences Building, Auburn University,
AL 36849-5407, USA. 2Department of Biology, Box 35-1800, University of Washington,
Seattle, WA 98195-1800, USA. 3Department of Biological Sciences, San José
State University, One Washington Square, San José, CA 95192-0100, USA. *Corresponding
author - boydrob@auburn.edu.
Soil and Biota of Serpentine: A World View
2009 Northeastern Naturalist 16(Special Issue 5):422–440
2009 R.S. Boyd, A.R. Kruckeberg, and N. Rajakaruna 423
mysteries. Today, however, ultramafics play a central role in the interpretation
of lithological sequences (ophiolite suites) at tectonic suture zones
worldwide. Ultramafic outcrops are now interpreted as originating from
upper mantle magma thrust upward to reach the surface of the earth’s crust.
A recent festschrift volume (Ernst 2004) honors the major contributions of
Robert Coleman, Professor Emeritus at Stanford University (California,
USA) and contributor to prior International Conferences on Serpentine
Ecology (Coleman and Alexander 2004, Coleman and Jove 1992), to this
reinterpretation of ultramafic geology.
Knowledge of ultramafic geology and soils is fundamental to serpentine
ecology (Alexander et al. 2007), and more information is needed to provide
an adequate foundation. Ultramafic rocks and soils are widely but patchily
distributed on Earth; they are found on every continent and in every
major biome (Harrison and Kruckeberg 2008). Some continents (Australia,
Europe, North America) are relatively well-studied, but many other areas
(Asia, Africa, South America) are comparatively unknown (at least to the
English-speaking world). The 6th Conference illustrated this imbalance, with
contributions regarding geology, soils, and plant/soil relations in the Appalachians
(USA), California (USA), Newfoundland and Québec (Canada),
Albania, Italy, and Puerto Rico. For example, in this Special Issue, D’Amico
et al. (2009) describe high-altitude serpentine soils of the Western Alps and
explore the correlations between soil metal concentrations and their biological
and microbiological activities.
But there were two notable exceptions at the 6th Conference to the
usual focus on Europe and North America. In one, a poster by Maria Marta
Chavarria Diaz (Area de Conservación Guanacaste, Costa Rica) and Earl
Alexander (Soils and Geoecology, Concord, CA, USA) presented information
on the serpentine geoecology of the Santa Elena Peninsula in Costa
Rica, thus building upon the pioneering exploration of Reeves et al. (2007)
into Costa Rican serpentine sites. The other exception, included in this
Special Issue (Cardace and Hoehler 2009), evaluates the ability of the serpentinization
process to create habitat capable of supporting microbial life.
This latter work is exciting for two reasons. First, the chemical reactions of
the serpentinization process may have generated conditions (including energy-
containing molecules such as methane or hydrogen) that promoted the
evolution of life on Earth (Schulte et al. 2006). Thus, serpentines may have
been the very cradle of biology! Second, Cardace and Hoehler (2009) are
exploring a similar connection between serpentines and life on other planets,
thus potentially taking serpentine ecology into the rarefied atmosphere
of interplanetary biology.
Serpentinologists are tempted to divide the world (geological,
pedological, and biological) in a binary way: “serpentine” versus “nonserpentine.”
But both serpentine sites and non-serpentine sites encompass
substantial variation, and the importance of this variation can be overlooked
in our desire to make generalizations. In particular, biologists and
424 Northeastern Naturalist Vol. 16, Special Issue 5
soil scientists tend to treat peridotite and serpentinite as “serpentine,”
but in fact the differences between those rocks may lead to important
pedological and biological distinctions. In this volume, Alexander (2009)
investigates this question and finds both soil and vegetation differences
between these two substrates in the Klamath Mountains of California–
Oregon, USA. Further studies that investigate variation in the geological,
pedological, and biological characteristics of serpentine areas, and
interactions between these categories of characteristics, are needed.
In addition, differences in soil characteristics and vegetation between
tropical and temperate-zone serpentine soils of similar overall chemical
composition are also worthy of more study.
Biota
As pointed out above, our knowledge of serpentine areas varies
greatly depending on their geographic location, and this is true for our
biological knowledge as well as our knowledge of geology and soils. At
the 6th Conference, contributions to our biotic knowledge of serpentine
areas included locations in Australia, Bulgaria, Canada (Newfoundland
and Québec), Iran, Italy, Japan, New Caledonia, Portugal, Russia, Spain,
Sri Lanka, Turkey, and the USA (California, Maryland, Pennsylvania,
and Maine). Some of these areas are better-studied than others, but there
is a long list of countries for which very little knowledge is available, at
least to the English-speaking scientific community. This caveat about the
English language is an important point; Brooks (1987) noted that about
30% of the serpentine literature used for his ground-breaking book was
written in languages other than English. Thus, we are unsure if our statement
above about the lack of knowledge regarding the serpentines of
some countries is due to our lack of familiarity with the content of non-
English language journals published in those countries. The areas lacking
serpentine research published in English includes those countries with
rapidly growing global influence, such as China and India, as well as the
countries of Central and South America. We hope that future International
Serpentine Conferences will include contributions from scientists in these
areas to achieve a truly global understanding of serpentine ecology.
An important outcome of each of the six International Conferences in
Serpentine Ecology has been the sharing of information between scientists
from different countries. In some cases, this sharing has included presenting
information in non-English languages (e.g., Jaffré et al. 1997, Boyd et al.
2004). Valuable as well are contributions in which the literature published in
one language is made available to readers of another by means of a review
written in that other language. A case in point is presented in this Special
Issue: the contribution of Mizuno et al. (2009) brings some of the serpentine
literature from a non-English speaking country (in this case, Japan) to the
attention of Anglophones.
2009 R.S. Boyd, A.R. Kruckeberg, and N. Rajakaruna 425
Future investigations that add to our knowledge of the serpentine biota
are sorely needed. Basic inventories are lacking for many relatively neglected
groups of organisms (e.g., bryophytes, insects, lichens, nematodes,
protists), and new species likely await discovery in these groups. As an
example, Figure 1 and the cover of this Special Issue show photos of Melanotrichus
boydi Schwartz and Wall, a new species of mirid bug described in
2001 that is found only on serpentines in the foothills of California’s Sierra
Nevada (Schwartz and Wall 2001). This species is one of the first discovered
“high-nickel insects,” species with relatively high levels of Ni in their tissues
that are currently known only from serpentine sites (Boyd 2009). Of
course, additional information is needed even in better-studied groups, such
as the vascular plants, and in relatively well-studied regions such as North
Figure 1. Adult form of the mirid bug Melanotrichus boydi, found only on serpentines
in the foothills of California's Sierra Nevada. Photograph © R. Boyd.
426 Northeastern Naturalist Vol. 16, Special Issue 5
America. Harris and Rajakaruna (2009) highlight several serpentine endemics
for eastern North America (including Adiantum viridimontanum; see
cover photo) and stress the need for additional surveys to better document
the biota of underexplored serpentine barrens of eastern North America.
Hyperaccumulators are fascinating plants that can take up relatively large
amounts of an element into their tissues. By now, over 390 taxa are known to
be Ni hyperaccumulators (Reeves and Adigüzel 2008), and the vast majority
of these grow on serpentine soils; Kazakou et al. (2008) report that 85–90%
of Ni hyperaccumulators are serpentine endemics, and the rest occur on
other soils but hyperaccumulate Ni when growing on serpentine soil. It is
likely that more are to be found in surveys of both temperate and tropical
serpentines, and these surveys must continue. At the Conference, Roger
Reeves (University of Melbourne, Australia) and Nezaket Adigüzel (Gazi
University, Ankara, Turkey) presented an update of their recently published
work (Reeves and Adigüzel 2008) documenting Ni hyperaccumulators from
the serpentines of Turkey and adjacent areas.
Many studies of serpentine biota use a comparative approach and evaluate
both serpentine and non-serpentine study sites. This approach was used
by two presentations at the Conference that add to our knowledge of ectomycorrhizal
(ECM) fungal communities (Branco 2009) as well as bryophytes
(Briscoe et al. 2009). The contribution of Branco (2009), included in this
Special Issue, investigates ECM associated with oak forests in Portugal,
finding evidence for potentially high fungal endemism in serpentine soils.
The bryophyte work of Briscoe et al. (2009), published elsewhere, reports
greater bryophyte diversity for serpentine compared to granite on the Deer
Isle complex, ME, USA.
Ecology and Evolution
Ecology
Serpentine outcrops often form ecological islands embedded in a matrix
of different rock types. Thus, they can be analyzed using the concepts of
“island biogeography,” as first outlined by MacArthur and Wilson (1967).
The pioneering work of Susan Harrison and colleagues (e.g., Harrison et al.
2006) has examined the California serpentine flora in just such a manner, but
more case histories are merited. Additional examples would be desirable,
from both temperate and tropical biomes (e.g., the Balkans, Brazil, Cuba,
etc.), to determine if different climatic or biogeographic factors in areas
other than California result in different biogeographic patterns.
Most serpentine sites worldwide make contact with non-serpentine
(“normal”) soil. Often there are noticeable differences in the soil and
vegetation (Fig. 2; Rajakaruna and Boyd 2008; see also this volume’s
cover photo of contact zone on Mt. Albert, Québec, Canada, taken on the
post-Conference field trip) and these differences have stimulated much
scientific interest in serpentine ecology. It is ironic, therefore, that these
2009 R.S. Boyd, A.R. Kruckeberg, and N. Rajakaruna 427
contact zones themselves are little investigated. What is the plant community
structure in such boundary zones? Are their soils intermediate in
chemical and physical properties? Does species composition in contact
zones differ from that of sites beyond the contact? Is there evidence for hybrid
swarms in such contact zones, especially of closely related taxa found
on the abutting substrates? We hope that future serpentine conferences will
include studies that seek answers to these questions.
Hyperaccumulator plants have received much attention in prior conferences
(e.g., Proctor 1999), and this trend continued at the 6th Conference.
Much research has focused on the physiology of hyperaccumulators (see
section on Physiology below), but the ecological interactions of hyperaccumulators
with other organisms are also being investigated. In recent
years, interaction ecology (plant-animal, plant-plant, etc.) has gained major
research attention. For serpentines, Robert Boyd and colleagues have
studied the impacts of Ni hyperaccumulation on species interactions in serpentine
communities. This work initially focused on plant interactions with
natural enemies, arguing that hyperaccumulation of metals could defend
plants against these natural enemies (see review from proceedings of the
5th Conference: Boyd 2007). It has expanded to explore other interactions,
including antagonistic plant-plant interactions (elemental allelopathy: see
review by Morris et al. 2009) and plant-decomposer interactions (Boyd et
al. 2008a). In this Special Issue, Boyd et al. (2009a) explore the impact of
hyperaccumulation on a commensal plant-plant interaction, showing that
bryophytic epiphytes in a New Caledonian humid forest have greater Ni
concentrations when they grow on Ni-hyperaccumulator host plants. They
also show that some of these bryophytes are themselves Ni hyperaccumulators
(as defined by the levels of Ni in the collected samples).
Many serpentine studies contrast serpentine and non-serpentine sites,
but as mentioned above, there is considerable ecological variation within
serpentine sites (Rajakaruna and Bohm 1999). Well known is the substantial
variation in chemical content (Ni, Ca/Mg, etc.) of serpentine soils.
Figure 2. Contact zone
between amphibolite
(on the left) and serpentine
(on the right)
at Mont Albert in Quebec,
Canada. Note the
strong vegetation differences.
Photograph ©
Ryan O’Dell.
428 Northeastern Naturalist Vol. 16, Special Issue 5
Examination of differences in species composition caused by differences in
soil chemistry would be desirable. A poster by Jennifer Doherty and Brenda
Casper (University of Pennsylvania, USA) explored arbuscular mycorrhizal
fungal (AMF) community diversity and how that diversity may affect performance
of serpentine grasses in heterogeneous serpentine soils. The Casper
lab is evaluating the role of AMF in plant-soil feedback (defined as influences
of a plant on soil properties that can affect the next plant to occupy the
same site) in Pennsylvania serpentine grasslands (e.g., Casper and Castelli
2007), finding that both feedback and plant-plant competition interact in
structuring these communities.
Evolution
Understanding plant adaptations to the “serpentine syndrome” has been
an important focus of serpentine ecologists for at least a half century. Years
ago, Anthony Bradshaw (Liverpool University, UK) found that certain
taxa from normal soils had the potential of incipient tolerance to soils with
high concentrations of heavy metals (Gregory and Bradshaw 1965). Such
pre-adaptation may also exist in taxa bordering serpentine sites. Simple
germination tests on serpentine soils could reveal preadaptation in certain
taxa. It may be proposed that such partial tolerance could be an initial step
towards ecotypic formation and subsequent speciation. Genera in certain tolerance-
prone families could be tested, e.g., Alyssum (madwort), Streptanthus
(jewelflower), Arabis (rockcress), Thlaspi (pennycress), and other genera in
the Brassicaceae, and in the Caryophyllaceae, genera like Silene (catchfly),
Minuartia (sandwort), and Dianthus (pink). Asteraceae and Poaceae are also
likely sources of testable taxa. Past studies have demonstrated that wideranging
species often have serpentine-tolerant and intolerant races. Nearly
all such cases have involved herbaceous genera. Yet to be tested are woody
species with serpentine and non-serpentine populations. Just for California,
genera like Adenostoma (chamise), Arctostaphylos (manzanita), Ceanothus
(ceanothus), Umbellularia (California laurel), Heteromeles (toyon), and
Garrya (silktassel) provide likely candidates for testing. Although many
taxa in these woody genera have long been considered as indifferent to
substrate, only common garden, ecophysiological, and genetic studies can
confirm if there is genotypic differentiation across substrate.
Studies of serpentine floras have noted “serpentinomorphoses,” morphological
differences between populations or taxa growing on serpentine
and non-serpentine soils (Kruckeberg 2002). These often include xeromorphic
features such as sclerophylly, reduced stature, and increased root:shoot
ratios (Kruckeberg 2002). At the 5th Conference, held on the serpentine-rich
island of Cuba, the contributions of our Cuban colleagues (e.g., Bécquer
Granados et al. 2004, Ferrás Alvarez et al. 2004) made plain this interesting
observation and also that the influence of serpentine environments on plant
form needs more study. What are the contributions of phenotypic plasticity
versus genetic traits to serpentinomorphoses? Exactly what are the
2009 R.S. Boyd, A.R. Kruckeberg, and N. Rajakaruna 429
ecological functions of serpentinomorphoses and how important are they
to adaptation to serpentine soils? In this Special Issue, Pavlova (2009)
documents variation between serpentine and non-serpentine populations of
Teucrium chamaedrys L., and Boyd et al. (2009b) explore morphological
and elemental concentration variation among populations of the serpentine
endemic Ni hyperaccumulator Streptanthus polygaloides Gray. We hope
that future Conference contributions will explore the evolutionary and
ecological ramifications of the variability documented by these and other
studies of serpentine plants.
How serpentine endemic species have evolved has tantalized botanists for
decades (Kruckeberg 1986, Rajakaruna 2004). Do they evolve directly from
non-tolerant species or from species that are already serpentine tolerant? At
the Conference, Brian Anacker et al. (University of California, Davis, CA,
USA) used molecular phylogenies to test whether serpentine endemic taxa
arise along a directional evolutionary pathway of non-tolerator to tolerator
to endemic. They reported several cases of significant directionality along
this hypothesized pathway, thus supporting this general model.
For areas already well inventoried, it would be desirable to determine
the relative ages of serpentine endemics. Are some taxa paleoendemics and
others neoendemics? The working hypotheses for ages of taxa are as follows
(Kruckeberg 2002): paleoendemics have no close relatives on nearby nonserpentine
sites; e.g., Darlingtonia californica Torr. (California Pitcherplant)
and Kalmiopsis leachiana (L.F. Hend.) Rehder (North Umpqua Kalmiopsis).
Neoendemics are thought to have close relatives on nearby normal soils:
e.g., California genera like Layia (tidy-tips), Streptanthus (jewelflower),
Gilia (gilia), and Phacelia (phacelia). These hypotheses need verification,
and the work of Anacker et al. presented at the Conference provided an initial
test; for their dataset from 20 genera, they found few endemic lineages
more than 10 million years old, suggesting that paleoendemics are relatively
rare. While this may be the case for the flora of California, it is important to
repeat such analyses, as phylogenies become available, for other serpentine
floras around the world.
Molecular phylogeny provides a unique protocol for testing and establishing
species relationships. As yet it has been little used to determine linkages
within genera having species on serpentine and normal soils (but see Baldwin
2005). Nearly every serpentine flora, temperate and tropical, has genera and
families suitable for phylogenetic verification. Among temperate genera, Alyssum,
Streptanthus, Thlaspi, and Phacelia would be worth testing. Numerous
genera found on serpentines of Cuba, New Caledonia, and South Africa could
be subjects for molecular phylogenetic study. Phylogenetic analysis has been
used to examine evolution of Ni hyperaccumulation in Alyssum (Mengoni et
al. 2003), serpentine tolerance in Calochortus (mariposa lily; Patterson and
Givnish 2004), and in angiosperms in general (Broadley et al. 2001), and similar
approaches could be used to assess patterns of serpentine endemism.
430 Northeastern Naturalist Vol. 16, Special Issue 5
Physiology and Genetics
Physiology
Questions still abound in the area of functional accommodation of plants
to serpentine soils. The question of Ca/Mg levels still provokes inquiry (Kazakou
et al. 2008). Is low Ca the major factor? Is high Mg a major player
in serpentine tolerance? It is not unlikely that species are more sensitive to
either low Ca or high Mg. Additionally, what is the importance of stresses
due to metals such as Co, Cr, and Ni? Given that a multiplicity of traits—
chemical and physiological—constitute Jenny’s “serpentine syndrome,”
experimental verification of serpentine tolerance will be complex. A recent
investigation (Oze et al. 2008) of elemental uptake into vegetation on serpentine
and non-serpentine (chert) soils suggested that elemental uptake
discrimination by roots is an important mechanism by which serpentine species
tolerate serpentine soil chemistry. It is likely that ecological as well as
physiological factors will be intertwined. For example, Springer et al. (2007)
showed that the susceptibility of Hesperolinon californicum Benth. (Small)
(California Dwarf-Flax; a species found both on and off of serpentine) to the
rust fungus Melampsora lini Persoon (Flax Rust) was negatively correlated
with soil Ca levels, suggesting that pathogen pressure on serpentine soils
would be more intense.
Major questions also abound at cellular and molecular levels. Mineral
uptake, translocation, or mineral exclusion must involve particular cellular
mechanisms (ATPases, protein transporters, etc.). Though progress has been
made in this area, further exploration of cellular/molecular mechanisms
is surely called for. At the 6th conference, there were few contributions
from scientists working in this area. One presentation, by Jola Mesjasz-
Przybylowicz and colleagues (iThemba Labs, South Africa), was unique in
that it examined Ni-elimination strategies by beetles feeding on a Ni-hyperaccumulator
plant, Berkheya coddii Roessler, from the serpentines of South
Africa. It was encouraging to see adaptive questions being asked regarding
serpentine animal species and thus broadening the focus from plants to other
serpentine biota. In this same vein, a poster presentation by Sonia Costa and
colleagues from the University of Coimbra, Portugal, examined mycorrhizal
colonization of a serpentine grass species as affected by Ni and soil fertility,
thus including plant-fungal interactions in this physiological session.
A most tantalizing conundrum in the area of mineral flux has to do with
Ni hyperaccumulation. Even though the number of Ni hyperaccumulators
is impressive (>390 taxa), many serpentinophytes either exclude Ni from
uptake or do not reach the hyperaccumulation threshold (>1000 mg Ni kg-1
in dry leaf tissue). Foremost is the question: how do most serpentine plants
prevent Ni uptake? This has to be a genetically fixed, adaptive trait. Answers
are likely to come from cellular and molecular methods. These approaches
are being used to determine the genetic bases and molecular pathways of
2009 R.S. Boyd, A.R. Kruckeberg, and N. Rajakaruna 431
hyperaccumulation; see the recent review by Verbruggen et al. (2009) for an
overview of our current understanding. Then, those taxa that can take up Ni
below the hyperaccumulation level pose other questions. Are these taxa on
the way to becoming hyperaccumulators? It can be hypothesized that those
few moderate Ni accumulators reveal the intermediate stages that Ni hyperaccumulators
could have gone through during their evolution. Boyd (2007),
proposing that defensive effects may be a selective force favoring survival
of plants with still higher Ni concentrations, called this the “defensive enhancement”
hypothesis for the evolution of elemental hyperaccumulation.
Evidence regarding this hypothesis is needed, and a presentation at the
conference of research by Sarah Dalrymple et al. (University of California,
Davis, CA, USA) showed that as little as 40 mg Ni kg-1 in shoots of Mimulus
guttatus DC (Seep Monkey Flower) reduced damage by caterpillar herbivores,
suggesting defensive effects of Ni at concentrations far less than
hyperaccumulator levels.
Several contributions in this Special Issue address other questions regarding
hyperaccumulation. Ghaderian et al. (2009) add to the extensive
early work of Homer et al. (1991) on metal uptake by Alyssum Ni hyperaccumulators.
Ghaderian et al. (2009) examine the ability of an Iranian Ni
hyperaccumulator (Alyssum bracteatum Boiss. and Buhse) to accumulate
Co, finding that plants from a serpentine population accumulate more than
those from a non-serpentine population. They also show Co hyperaccumulation
is possible when plants are grown in an artificial medium, suggesting
that Ni and Co uptake and sequestration abilities are correlated. Pollard et
al. (2009) investigate the ability of a non-serpentine species (Phytolacca
americana L. [Poke Sallet]) to take up Mn. They find that, under hydroponic
conditions, plants hyperaccumulate Mn even though no cases of hyperaccumulation
have been reported from plants in the field. They thus document
what Boyd and Martens (1998) termed “latent hyperaccumulation,” the
physiological ability of a species to hyperaccumulate that is not detected by
studies of field-collected samples. Field-collected samples are part of the
definition of hyperaccumulation (see Reeves 1992), but Pollard et al. (2009)
show that there may be more species of plants with hyperaccumulation
abilities than we had thought. Boyd and Jaffré (2009) examine the influence
of leaf age on Ni concentration in New Caledonian serpentine species,
including species that cover a wide range of leaf Ni levels. They report that
leaves generally do not vary significantly in Ni levels as they age. They also
suggest use of a new term (hemi-accumulator) to categorize plants with Ni
levels in the range of 100–1000 mg Ni kg-1 (in dry leaf tissue), to complement
terms currently in use for plants with <100 mg Ni kg-1 (non-accumulator),
1000–10,000 mg Ni kg-1 Ni (hyperaccumulator), and >10,000 mg Ni kg-1
(hypernickelophore). Finally, Mesjasz-Przybylowicz et al. (2009) study the
ultrastructure of roots of the South African Ni hyperaccumulator Senecio
coronatus (Thunb.) Harv. This species is unusual because some serpentine
432 Northeastern Naturalist Vol. 16, Special Issue 5
populations hyperaccumulate Ni whereas others do not (Boyd et al. 2008b);
only a few Ni-hyperaccumulator species show this variation in Ni hyperaccumulation
(Kazakou et al. 2008). Mesjasz-Przybylowicz et al. (2009) report
several differences, including differences in the Casparian strips, that may
help explain the ability of the non-hyperaccumulator to limit Ni uptake from
serpentine soil.
Genetics
The long-standing question of the genetic basis for serpentine tolerance
has yet to be fully resolved: is tolerance controlled by a single or few
genes or is it polygenic? Approaches to solving this question could involve
breeding tests, DNA analyses, and other techniques. For example, the Toby
Bradshaw lab (University of Washington, Seattle, WA, USA) is exploring
this question (Brady et al. 2005) for species in the genus Mimulus (monkey
flower) using quantitative trait loci (QTL). The evolutionary ecology of
serpentine endemism is also the target of “serpentinomics,” the application
of genomic techniques to analyze local adaptation (Wright and von Wettberg
2009). Wright and von Wettberg (2009) present their efforts to detect
molecular convergence among multiple Collinsia sparsiflora Fisch. & C.A.
Mey. (Spinster's Blue-eyed Mary) populations that have adapted to serpentine
soils. This work builds on initial work that used F2 hybrids to analyze
patterns of local adaptation and selection on serpentine and non-serpentine
populations of this species (Wright and Stanton 2007). Genomic tools are
also important to discern relations among the microbe populations found
on and off of serpentine soils. A recent study employs such tools to explore
patterns of microbial diversity and biogeography across serpentine and nonserpentine
substrates (Oline 2006).
We mentioned previously the general lack of ecological information
regarding serpentine/non-serpentine contact zones, and genetic questions regarding
these zones have also not yet been explored. For example, how much
and to what effect does gene flow into or from serpentine and normal soils
have on populations on either side of the edaphic boundary? Techniques exist
for facilitating such studies: aerial insect transmission of tagged pollen,
marker genes in either population, or detection of enhanced serpentine tolerance
in neighboring non-serpentine populations.
Applied Ecology
The effects of human activities on serpentine sites have been substantial
and have worked reciprocally. Serpentines have impacted humans, and even
more so, human intrusions on ultramafics have gone on for centuries (Kruckeberg
2002). There are several research directions needed here. Physical
alteration of serpentine sites (mining, logging, fire, etc.) post still unresolved
issues. Can disturbed serpentines be restored, especially by planting tolerant
plant stock? How do native species on serpentines react to disturbance?
2009 R.S. Boyd, A.R. Kruckeberg, and N. Rajakaruna 433
Some species may increase under disturbance, while others decrease or
even become extinct. Revegetation of disturbed serpentine sites has been an
important theme in past conferences; for example, the proceedings of the 2nd
International Conference (Jaffré et al. 1997) contained an entire section of
nine papers dedicated to this topic. In this Special Issue from the 6th Conference,
O’Dell and Claassen (2009) provide a review of the concepts involved
in revegetating disturbed serpentine sites. Their paper is a helpful summary
of the literature in this applied area of serpentine ecology. A specific environmental
hazard associated with some serpentine sites is that associated with
asbestos. Favero-Longo et al. (2009) report results from using native plants
to reduce the hazards of airborne asbestos fibers originating from a closed
serpentine mining site. They find that plant cover significantly reduces the
hazard and provide an example of how successful revegetation can yield
important environmental benefits.
The growing human population of the planet drives humanity to consider
ways to generate new arable land. Can serpentine habitats be brought into
productive agriculture? Because of the challenges of the “serpentine syndrome”
for plant growth, these areas are not often used for traditional crops.
Yet some crops are grown successfully on managed serpentine soils (e.g.,
growing wine grapes on serpentine alluvial soils in California). Our understanding
of the “serpentine syndrome” and its effects on plants may suggest
agricultural strategies that can put some serpentine soils into agricultural
use. A non-traditional agricultural technique that may use plant species native
to serpentine is phytomining (Nicks and Chambers 1998). For example,
in this technique, a Ni hyperaccumulator would be cultivated on serpentine
soils, harvested, and processed into ore for its Ni content. Some initial tests
of the feasibility of this technology have been conducted (e.g., Brooks et al.
2001). A kindred use of serpentine species is in the field of phytoremediation
(Raskin and Ensley 2000, Pilon-Smits 2004). Barely tested is the possibility
of using hyperaccumulators to extract metals from contaminated sites (Rajakaruna
et al. 2006). These extracted metals could then be processed into
ore as in phytomining, or even be useful as food supplements in the case of
Zn (Mayer et al. 2008), since Zn is an important dietary micronutrient. However,
from the conservation perspective, it is critical that such phytomining
operations are established on degraded serpentine landscapes rather than on
pristine habitats.
Conservation of serpentine biota is another important area of concern
(Rajakaruna et al. 2009). The need for conservation of these unique areas
was recognized at the First International Conference on Serpentine Ecology,
held in 1991 at the University of California, Davis, CA, USA. The 70 delegates
to that conference approved a resolution calling upon governments,
public and private agencies, and private industry to take steps to protect the
biodiversity contained in serpentine areas (Kruckeberg 1992). This call has
been repeated since then (e.g., Whiting et al. 2004) and remains an area in
need of close attention.
434 Northeastern Naturalist Vol. 16, Special Issue 5
A major problem in conservation biology is the impact of non-native invasive
species on natives (Terrill 2007), and disturbed serpentine sites can be
invaded by weedy species of non-serpentine origin. There is some evidence
(Harrison et al. 2003) that serpentine habitats have fewer non-native plant
species, presumably because they are challenging media for plant growth.
Are successful non-native invasive species ones that are already genetically
tolerant, either by possessing a general-purpose genotype or by rapidly
evolving tolerance? And how do other anthropogenic changes alter the invasibility
of ultramafics? For example, recent studies (Weiss 1999, Zavaleta
et al. 2003) show that vehicle emissions have resulted in N-enrichment of
serpentine soils near major California highways. This enrichment may allow
non-native species to invade these ultramafic sites by alleviating N limitation
in these soils. A similar but important area of research should focus on
multiple nutrient and other element enrichment via atmospheric sources. The
deposition of other nutrients such as P and Ca and various pollutants can
also have drastic impacts on the unique soil chemistry and resulting biotic
interactions of serpentine habitats.
Climate change is predicted to affect the planet’s biota in major ways
(Loarie et al. 2008, Thomas et al. 2004), and recent analysis (Solomon et
al. 2009) suggests it may be irreversible on a timescale of a millennium or
so. Edaphically restricted communities such as those on serpentine sites
will be affected as well. But will the features that make them unique, such
as their insular nature and their biogeochemical/biological distinctiveness,
make them more or less susceptible to disruption by climate change? Harrison
et al. (2009) propose a conceptual model to test this question and are
gathering long-term comparative data to provide initial answers. Additional
studies in other geographic regions would be helpful; in particular, the history
of scientific interest in European serpentine areas (Brooks 1987) may
allow for other long-term datasets to be generated there. In the context of
serpentine endemism, we speculate that narrow endemics are more liable to
extinction due to climate change. Since some narrow endemics are already
endangered by their limited ranges, climate change will likely increase
their chances of extinction.
A major driver of climate change is carbon emissions into the atmosphere
(Hansen et al. 2008, Solomon et al. 2009). Given the potential threat of climate
change to the serpentine flora, it is ironic that serpentine sites may offer
a partial solution to climate change by providing a mechanism for carbon sequestration.
Extremely Mg-rich rock, such as olivine or serpentine, can react
with water and carbon dioxide to form magnesium carbonate plus silica, thus
sequestering potentially damaging carbon dioxide emissions (Maroto-Valer
et al. 2005). This technique is under investigation (see review by Yang et
al. 2008), but it is unclear how its large-scale application might impact the
biota of serpentine areas. If the overall history of human impacts on Earth’s
habitats is any guide, this partial solution to climate change could severely
impact serpentine sites used to implement this technology. It would be tragic
2009 R.S. Boyd, A.R. Kruckeberg, and N. Rajakaruna 435
to be forced to degrade the biodiversity of serpentine sites in order to help
save biodiversity on a planetary scale. As we mentioned earlier, scientists
have speculated that serpentine vents may have been involved in the initial
evolution of life on Earth. It would be an irony of cosmic proportions if the
biota of present-day serpentine sites were to be sacrificed in order to help
save the life formed on Earth billions of years ago during serpentinization!
Summary
By the early 21st century, studies on the geology and biology of ultramafics have become a significant focus in the natural sciences. Yet inevitably,
the burgeoning fields of research have unearthed yet more unresolved questions.
Our mission here has been to describe some of the challenges awaiting
future research and some of the contributions made during the 6th International
Conference on Serpentine Ecology. We hope that the 7th International
Conference (scheduled for 2011 and hosted by the University of Coimbra
in Portugal) will be as successful as the 6th (and prior) Conferences were in
advancing our knowledge of these fascinating areas. Certainly, the new generation
of serpentinophilic scientists has a full palette from which to choose
their research questions!
Acknowledgments
We thank Professors Alan J.M. Baker and Susan Harrison for helpful comments
on the original manuscript.
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