Ecology of the Deep Bryophyte Community in Crater Lake, Oregon
Abstract
An extensive biological community associated with submerged mosses,
discovered by submarine in 1988 and 1989, though invisible from the
lake surface, forms a band around the lake between 25 and 140 meters in
depth that may dwarf other components of the ecosystem in biomass, and
provide a critical link in nutrient cycles between terrestrial,
benthic, and open-water components of the ecosystem. While a large area
in the depth range of the moss beds is blanketed with deep mats of
cryptogamic macrophytes, certain areas show clear signs of recent
deterioration of the living mats, and living shoots in those areas are
sparse or entirely absent. It appears that a large area of the
bryophyte mat community has declined in recent decades before their
role in the ecology of the lake can be studied. At the same time there
is increasing evidence that the deep bryophyte community contains the
largest fraction of standing biomass in the lake, and may have a
critical role influencing both biodiversity in the lake and nutrient
chemistry.
Understanding the spatial distribution, biomass, and role in
carbon/nitrogen budgets of the deep-water bryophyte community in Crater
Lake was identified as a research priority by the Crater Lake Long-Term
Limnological Monitoring Program peer review panel in 2000. The panel
prioritized six research objectives, including “continued research on
the nutrient balance for the lake, especially the [problem of] missing
nitrogen," and testing the hypothesis that "deep-water moss. . .acts as
an important nitrogen sink." Understanding the ecological structure and
function of the deep bryophyte community is clearly critical for a
comprehensive description and understanding of the lake’s aquatic
ecosystem. Understanding the mechanisms behind the apparent decline of
the bryophyte community over large areas is necessary to interpreting
how those changes will affect lake ecology as well as providing
baseline information for monitoring and mitigating undesirable changes
in the lake ecosystem.
We propose to 1) describe in detail the species composition and species
abundances of macrophytes in the deep bryophyte community, and perform
a detailed inventory of the associated cyanobacteria, autotrophic and
heterotrophic protists, and invertebrates associated with both living
and declining bryophyte mats; 2) develop a classification of bryophyte
mats as characterized by standing biomass, sedimentary profiles,
composition and complexity of the living components; 3) characterize
differences between living, declining, and dead bryophyte mats in terms
of community composition, structure and function, with function
measured in terms of growth rates of dominant species in different mat
types; 4) test hypotheses explaining the upper limits of mat formation
using in situ manipulation of samples in growth chambers; 5) provide
ground-truthing for results from the multi-beam high-resolution sonar
backscatter analyses with independent estimates of standing biomass
that will help to calibrate results from that study; 6) develop a
detailed mapping of mat types showing the spatial distributions of
different mat types, their present conditions, and the arial extent of
living, declining, and dead mats.
Justification
Limnological studies of Crater Lake from 1982 to 2002 focused on
physical, biological, and chemical processes in the offshore
environment of the lake. A unique combination of climate, geology, and
morphology result in one of the clearest and deepest ultra-oligotrophic
(nutrient poor) lakes in the world. The extremely clear water,
and associated increased light penetration, account for unusually deep
distributions of aquatic plants and animals. Crater Lake is nutrient
poor because inputs of water and nutrients are limited to direct
atmospheric deposition to the lake, and runoff from the steep caldera
walls. Nutrient studies indicated that up to 90% of the annual nitrogen
budget in the upper lake comes from deep lake upwelling driven by
winter storms. Recycling of nutrients by the biological community
(bacteria, phytoplankton, zooplankton, and fish) result in
approximately 10% lost to the deep lake annually. However, nutrient
inputs to the lake are estimated to be 2 to 10 times greater than could
be accounted for by open water processes measured with mid-lake
sediment traps. One hypothesis for this discrepancy is that biological
productivity along the caldera walls and Wizard Island is relatively
high and that associated detritus is transferred from the lake margins
to the deep lake by sloughing of organic material.
A remarkable deep-water bryophyte community in Crater Lake, found
living at depths between 25 and 140 m, may comprise most of the biomass
in the lake ecosystem (McIntire et al., 1994), yet community
composition and structure, spatial distribution, growth rates, and
ecosystem function of the deep bryophyte community are virtually
unknown. McIntire et al. (1994) identified one of the dominant species
as, Drepanocladus aduncus
Warnst., a moss that was recorded in earlier, mostly unpublished
reports of benthic bryophytes in the lake. The only other bryophyte
reported from the lake to date (Hasler 1938; Brode 1938) is Fontinalis howellii Ren. &
Card. (= F. antipyretica var.
oregonensis Ren. & Card.). Bryophyte samples from the lake
examined by S. Jessup in a preliminary study conducted in 2001
(unpublished data communicated to M. Buktenica, 7/25/01) were found to
have several additional species, including Fissidens fontanus (Pyl.) Steud., Fontinalis neomexicana Sull. &
Lesq., Leptodictyum riparium
(Hedw.) Warnst., Platydictya
jungermannioides (Brid.) Crum, Platyhypnidium
riparioides (Hedw.) Dix., Hygrohypnum
ochraceum (Wils.) Loeske, and traces of Cephaloziella uncinata Schust., the
first liverwort reported from the deep bryophyte community of Crater
Lake. Bryophyte mats sampled in Fumerole Bay are formed by massive
accumulations of Leptodictyum riparium, whereas samples from other
locations were dominated by other species or were mixtures of other
species. Mats in Fumerole Bay and elsewhere in the lake appear to have
ceased active growth in recent decades. Preliminary studies reveal
living cells in leaves at the stem tips, but apparently little or no
recent growth. While preliminary study has been limited to just a few
samples, a substantial increase in the number of species known from the
aquatic bryophyte community in the lake, and a clearer view of an
apparently recent decline in growth of the moss mats has resulted. The
preliminary results suggest 1) that the bryophyte community is more
diverse than previous studies have shown, 2) that species composition
of the bryophyte community in the lake varies substantially from one
site to the next, and 3) that recent changes the structure and function
of the deep bryophyte community might have resulted in the large areas
of dead and declining bryophyte mat that have been observed.
The preliminary studies, however, raise more questions than they
answer, and the need for a focused study is indicated. In particular, a
comparative analysis of living, declining, and dead bryophyte mats
would answer questions of central relevance to an understanding and
modeling of the lake ecosystem, while also providing a baseline of
information useful to managers in making decisions relevant to health
of the lake ecosystem.
The ecological role of the deep bryophyte community in lake chemistry,
specifically its significance in the nutrient budget of this
ultra-oligotophic ecosystem, is essentially unknown (McIntire et al.,
1994), but given the large standing biomass it is thought to be an
integral component of lake ecosystem function. The lake ecosystem is
nitrogen-limited, and the deep bryophyte community may function as a
nitrogen sink (Dymond and Collier, 1993). Since a large fraction of the
biomass in the lake apparently resides in accumulated living mats of
bryophytes, periodic deep mixing of nutrients into the euphotic zone
could result in rapid sequestration in the bryophyte community.
Detrital accumulation of bryophytes sloughed from the caldera walls
into abyssal sediment pockets in the lake might function as a long-term
sink for nitrogen, effectively removing it from circulation.
Understanding ecosystem function of the deep bryophyte community
requires estimating growth rates as a function of physical and chemical
features of the environment that vary with depth. Although the depth
distribution of aquatic angiosperms is typically limited to a maximum
depth of 15 m (Hutchinson 1975), deep-water vegetation in
ultra-oligotrophic lakes (primarily mosses, liverworts, and algae) have
depth maxima of approximately 118-140 m (Brode 1938; Hasler 1938;
Frantz & Cardone 1967; Drake et al. 1990; McIntire et al. 1994;
Wagner et al. 2000). The lower limit of the moss depth distribution is
generally attributed to light limitation, occurring at 0.10-0.13% of
surface irradiance (Frantz and Cordone 1967; McIntire et al. 1994), and
is thus sensitive to changes in lake clarity and optics. The
constraints imposing the upper limit of the moss depth distribution
(25-30 m) are more enigmatic. The minimum depth of moss in Crater Lake
may be imposed by thermal tolerances, exposure to UV light,
photoinhibition, photorespiration, substratum-type and availability,
nutrient limitation, competition with phytoplankton, disturbance
regimes, or some combination of these. One hypothesis (McIntire et al.
1994) attributes the upper limit to summer depletion of nitrogen in the
epilimnion when temperatures are sufficient for photosynthesis, while
mixing of the hypolimnion keeps nitrate in the lower euphotic zone
throughout the summer.
The proposed study will test several hypotheses attributing attenuation
of bryophyte distribution at both the upper and lower depth limits to
physical and chemical constraints on growth. The study will measure in
situ growth rates of the dominant species across their depth
distributions, with various manipulations of environmental factors. If
growth limitation in response to physical/chemical constraints
regulates depth distribution, then growth rates should decline near the
limits of distribution, and experimental samples placed at depths
outside the natural limits should demonstrate absence of growth. Growth
rates will be measured in situ as net annual shoot production (ASP), as
indicated by measured increases in dry weight of shoot apices (Longton
1980) or simply as increases in number of leaves initiated during a
fixed interval (Sand-Jensen et al. 1999). The effect of simple shading
and UV-filtering experiments on growth rates will be used to test the
hypothesis that photoinhibition plays a role in the upper depth
limitation. If experimental samples placed at upper depths with shading
and UV filtering exhibit absence of growth, then nutrient limitation is
the most likely limiting factor. Experimental manipulations of
nutrients within closed growth pods incubated in situ at various depths
will be used to isolate the effects of nutrient limitation. Since peak
annual surface temperatures (15-20º C) are near optimal for net
photosynthesis in many mosses, temperature limitation is unlikely. For
example, Collins (1977) found that net photosynthesis was optimum at
20º C in Antarctic populations of Drepanocladus uncinatus, a close
relative of one of the Crater Lake dominant species, D. aduncus. In
studies of another close relative of a Crater Lake species, however,
Glime and Carr (1974) documented mortality in winter-acclimated
Fontinalis novae-angliae at temperatures exceeding 15º C. It is
possible that depth distributions of some species in the deep bryophyte
community are constrained by temperature while others are constrained
by photoinhibition or nutrient limitation. The experimental protocol
will replicate growth measurements for each of the dominant species.
Samples collected for growth rate studies will be incubated in situ on
tethered arrays of growth rate measurement devices.
The living part of the deep bryophyte community is built on accumulated
nonliving biomass that forms a dense mat in places. The study proposed
here complements a sister study funded in 2002 (entitled “Application
of multi-beam high-resolution sonar data to characterize the habitat,
spatial distribution, biomass and ecological significance of deep-water
aquatic vegetation”). That study will combine use of recently-collected
data from a high-resolution multi-beam sonar survey (Gardner, et al.,
2000) with a carefully targeted field study of the deep bryophyte
community in the caldera. The field component of that study will use a
remotely-operated vehicle (ROV) dive program to ground-truth habitat
models and sonar backscatter observations. Data from that project will
inform sampling strategies in this project that are aimed at assessing
rates of biomass accumulation. Results obtained from the ROV imaging of
mats in 2006 will provide information needed to target specific mat
types for ground-truthing with samples for laboratory analysis.
Mosses generally have slow rates of decomposition relative to vascular
plants (Longton 1980; Sand-Jensen et al. 1999), and under low
temperature conditions biomass accumulation may greatly exceed rates of
decomposition, even when primary production is quite low. Consequently,
bottom layers of the resulting mat may be very old. Since the balance
of rates of production and decomposition is the rate of biomass
accumulation, if we can estimate both growth rates and standing biomass
in terms of stem lengths, and show how biomass per unit stem length
changes from the top to the bottom of the mat, we can then estimate
both the age of the mats and rates of decomposition. Morphology in
living stem sections of the dominant species will be examined for
indicators of annual growth (such as intervals of leaf or gametangia
initiation). The combined data from this study and the sister study
will provide estimates of standing biomass, net annual biomass
accumulation, and rates of decomposition in the deep bryophyte
community.
The physical structure of living bryophyte mats likely provides habitat
for a diverse biota of photosynthetic and non-photosynthetic
prokaryotes, protists, and invertebrates. Early characterizatoin of
community compositon of these diverse biotic assembleges (McIntire et
al. 1994) was largely limited to epiphytic algae. Next to nothing is
known about how characteristics of the bryophyte mat affect structure,
function and complexity of the associated microbiota. In particular, it
would be helpful to development of management objectives to understand
how complexity of the associated biota varies across mat type, mat
health, and mat depth. The comparative analysis of associated biota in
this study will help to characterize mat types and provide information
about how characteristics of mat health, particularly physical
structure of the mats and growth rates, influences biodiversity of
microorganisms within the lake.
A possible sink for both carbon and nitrogen is deep burial of biomass
from the bryophyte community sloughed from steep walls of the caldera
into abyssal sediments. Detrital bryophytes have been collected below
200 m, and may form deep pockets of sequestered biomass below areas of
high biomass accumulation in the living community (McIntire et al.
1994). Although sediment cores from Crater Lake have been screened for
pollen and diatoms (Nelson 1994) there are no published reports of
bryophytes from Crater Lake sediments, though they are typically found
in similar deep lacustrine sediments (Miller 1980, 1984). There have
been no targeted attempts to recover sediments from areas where
bryophyte detritus is likely to accumulate. In the proposed study,
existing sediment samples and cores from targeted areas would be
re-examined for bryophyte remains, and any discovered remains would be
identified. New sediment samples will be obtained from areas where
sloughing is likely to result in deep pockets of detrital bryophyte
biomass. Sites targeted for exploration are those where large biomass
accumulations are found on steep underwater terrain directly above the
deep basins.
The deep bryophyte community is a promising bioindicator of ecosystem
health and stability in Crater Lake. Factors contributing to decline
and death of bryophyte mats are not at all understood. Whether natural
or anthropogenic, the declining mats probably indicate a major shift in
community compositiona and ecosystem structure and function. Baseline
data is needed to monitor changes in this substantial component of the
lake ecosystem, and to provide for informed management decisions.
Identifying the suite of factors that constrain the health and
distribution of the deep bryophyte community will facilitate
understanding how lake temperature, lake clarity, and nutrient cycling
affect this important component of the lake biota, and provide a useful
tool for monitoring and evaluating change in the lake ecosystem.
Criteria:
Significance of Resource at Risk – Crater Lake is the primary landscape
feature responsible for the establishment of Crater Lake National Park.
It’s pristine water and unique biological, chemical, and physical
attributes make Crater Lake an international study site for processes
common to lake and ocean environments worldwide. A long-term monitoring
program is in place to develop a comprehensive understanding of the
lake ecosystem and to track change relative to local, regional, and
global influences. An understanding of the distribution and function of
submerged plant, bryophyte, and microorganism communities is a critical
part of the comprehensive description of an aquatic ecosystem. In the
case of Crater Lake, a remarkable deep-water moss community appears to
represent the bulk of the biomass in the lake ecosystem, yet its
community composition and structure, arial distribution and ecological
significance is poorly quantified. The deep bryophyte community is a
promising bio-indicator of ecosystem health and stability in Crater
Lake. Specifically, large areas of bryophyte mats, covering the
substratum to several meters in thickness, appear to have undergone
recent decline in growth and vigor. Identifying the suite of factors
that constrain the health and distribution of the deep bryophyte
community will provide a powerful tool for evaluating spatial-temporal
variability in the distribution and abundance of biomass in the lake,
and thus for assessing ecosystem change. Knowing the community
composition of the mat organisms and associated microbiota and rates of
growth and primary production of mat bryophytes in the lake will allow
researchers to better evaluate the role of the deep bryophyte community
in nutrient cycling and energy flow through the ecosystem. Comparison
of healthy and declining bryophyte mats will provide a valuable source
of information for assessing management options should the mats
continue to decline. Without baseline data, however, fundamental
changes in lake ecosystem structure and function may not be apparent
until it is too late for management interventions.
Although this project will physically occur in one park the resulting
knowledge relative to aquatic ecosystem function would have widespread
application. The study will provide a significant contribution to
global understanding of how deep lacustrine bryophyte communities
function in the ecology of ultraoligotrophic lakes by elucidating the
role of such communities in influencing ecosystem biological-chemical
cycling and food-web structure.
Severity/Urgency of Response – Understanding the Crater Lake ecosystem
and preserving Crater Lake are paramount to the management of Crater
Lake National Park. While preliminary results showing large areas of
bryophyte mat in decline are inconclusive, these observations may
indicate a trend, natural or otherwise, within the lake ecosystem. This
project will fill a crucial gap in our knowledge that could be applied
directly to understanding lake processes and will provide a foundation
of baseline knowledge needed to evaluate the significance of changes in
lake ecology. The investigation of the distribution, biomass, and role
in carbon/nitrogen budgets of the deep-water bryophyte community in
Crater Lake has been clearly identified as a research priority by the
Crater Lake Long-Term Limnological Monitoring Program peer review panel
(CRLA LTLMP peer review report, 3/31/00). The six research activities
prioritized by the panel included "continued research on the nutrient
balance for the lake, especially the [problem of] missing nitrogen,"
and the investigation of the hypothesis that "the deep-water moss could
act as an important nitrogen sink."
Prospect for Problem Resolution – The proposed study uses
well-tested protocols and limnological methods to address questions
that are fundamental to understanding ecology of the Crater Lake
ecosystem. Protocols for sampling and inventorying community
composition, measuring growth rates, and data analysis planned for this
study are standard practice in limnology (Wetzel and Likens, 3rd
edition 2000, Wetzel, 3rd edition 2001). Techniques for measuring
growth rate of bryophytes have been specifically reviewed by Longton
(1980), and the methods planned for this study are especially well
suited for aquatic bryophytes which typically have lax stems with loose
branching patterns. The PI Jessup, a former research assistant at the
University of Maryland, Horn Point Laboratory, with two years of
graduate study in phytoplankton ecology at the University of Rhode
Island, School of Oceanography, has considerable experience with
bryophytes and brings his professional training in aquatic ecology to
bear on the problem as well.
This study will augment the currently funded project, "Application of
multi-beam high-resolution sonar data to characterize the habitat,
spatial distribution, biomass and ecological significance of deep-water
aquatic vegetation." Field work will commence in 2006 with seed funding
awarded the PI's by the Crater Lake Natural History Association. The
PI's will submit a proposal to NSF with data from this project in Year
2 for funding to continue research on the role of the deep bryophyte
community in ecology of the lake ecosystem. Together the two projects
provide a synergistic view of lake ecology in Crater Lake that will
substantially advance our knowledge of the system.
Investigators:
Steven Jessup, Ph.D., Associate Professor, Department of Biology,
Southern Oregon University, Ashland, OR 97520. (541) 552-6804 [voice],
(541) 552-6415 [fax], jessup@sou.edu.
Mark Buktenica, Aquatic Ecologist, Crater Lake National Park, PO Box 7,
Crater Lake OR 97604. (541) 594-3077 [voice], (541) 594-3050 [fax],
mark_buktenica@nps.gov Adjunct Faculty in Biology, Southern Oregon
University, Ashland, OR 97520, (541) 552-8301 [voice], (541) 552-8301
[fax], buktenim@sou.edu
Literature Cited:
Brode, J.S. 1938. The denizens of Crater Lake.
Northwest Science 12: 56-57.
Collins, N.J. 1977. The growth of mosses in two contrasting communities
in the maritime Antarctic: measurement and prediction of net annual
production. Pp. 921-933 in G.A. Llano (ed.) Adaptations within
Antarctic Ecosystems. Smithsonian Institution, Washington, D.C.
Drake, E., G.L. Larson, J. Dymond, and R. Collier. 1990.
Crater Lake: an ecosystem study. Ammer. Assoc. Adv. Sci.,
California Academy of Sciences, San Francisco.
Dymond, J., R.W. Collier. 1993. Particle flux
measurements. In G.L. Larson, C.D. McIntire, and R. Jacobs (eds.)
Crater Lake Limnological Studies Final Report. U.S. National Park
Service.
Frantz, T.C., A.J. Cordone. 1967. Observations on deep-water
plants in Lake Tahoe, California and Nevada. Ecology 48:709-714.
Gardner, J.V., L.A. Mayer and M. Buktenica 2000. Mapping the bathymetry
of Crater Lake, Oregon. US Geol. Survey Open-File Rept. 00-405, 31p.
http://geopubs.wr.usgs.gov/open-file/of00-405/
Glime, J.D. 1974. Temperature survival of Fontinalis novae-angliae
Sull. Bryologist 77:17-22.
Hasler, A.D. 1938. Fish biology and limnology of Crater
Lake, Oregon. Journal of Wildlife Management 2:94-103.
Hutchinson, G.E. 1975. A treatise on limnology. Vol.
3. Limnological Botany. John Wiley and Sons, New York.
Longton, R.E. 1980. Physiological ecology of mosses. In R.J. Taylor
& A.E. Leviton (eds.) The Mosses of North America. Pacific
Division, AAAS.
McIntire, C.D., G.L. Larson, M. Buktenica. 1994. Vertical
distribution of a deep-water moss and associated epiphytes in Crater
Lake, Oregon. Northwest Science 68(1):11-21.
Miller, N.G. 1980. Fossil mosses of North America and their
significance. In R.J. Taylor & A.E. Leviton (eds.) The Mosses of
North America. Pacific Division, AAAS.
Miller, N.G. 1984. Tertiary and Quaternary fossils. Pp. 1194-1132 in
R.M. Schuster (ed.) New Manual of Bryology, Vol. 2. Hattori Botanical
Laboratory, Nichinan, Miyazaki, Japan.
Nelson, C.H., C.R. Bacon, S.W Robinson, D.P. Adam, J.P. Bradbury, J.H.
Barber, D. Schwartz, G. Vagenas 1994. The volcanic, sedimentologic, and
paleolimnologic history of the Crater Lake caldera floor, Oregon:
evidence for small caldera evolution. Geological Society of America
Bulletin 106:684-704.
Sand-Jensen, K., T. Riis, S. Markager and W. F. Vincent 1999. Slow
growth and decomposition of mosses in Arctic lakes. Can. J. Fish.
Aquat. Sci. 56(3): 388-393.
Wagner, D.H., J.A. Christy and D.W. Larson 2000. Deep-water bryophytes
from Waldo Lake, Oregon. Lake and Reservoir Management 16:91-99.
Wetzel, R. G. 2001. Limnology: Lake and River Ecosystems, 3rd Edition.
Elsievier Academic Press. 1006 pp.
Wetzel, R. G. and G. E. Likens 2000. Limnological Analyses, 3rd
Edition. Springer. 429 pp.
Collecting cryptogams on Phantom Ship,
in the Crater Lake Caldera, Crater Lake National Park
