Forest Canopy Research: Sampling Problems, and Some Solutions Author(s): Martin G. Barker and Michelle A. Pinard Source: Plant Ecology, Vol. 153, No. 1/2, Tropical Forest Canopies: Ecology and Management. Proceedings of the European Science Foundation Conference, Oxford University 12-16 December 1998 (Apr., 2001), pp. 23-38 Published by: Springer Stable URL: http://www.jstor.org/stable/20051044 Accessed: 21/09/2009 04:41 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=springer. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact
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Plant Ecology 2001 Kluwer
?
Forest
153:
23-38,2001. Academic Publishers.
research:
canopy
in the Netherlands.
Printed
sampling
Martin G. Barker1 & Michelle
and
problems,
some
solutions
A. Pinard2
1 Department of Plant and Soil Science, University of Aberdeen, Cruickshank Building, Aberdeen AB24 3UU, UK (E-mail:
[email protected]);2 Department of Forestry, University of Aberdeen, MacRobert Building, Aberdeen AB24 5UA, UK
Key words: Canopy
access, Replication,
Sample, Tree crowns
Research methodology,
Abstract Conducting research in forest canopies is accompanied by both opportunities and difficulties. Opportunities occur because the canopy is important in overall forest structure and function, for example in containing a high proportion of species richness, being the site of forest-atmosphere fluxes, and in strongly influencing understory microclimate. However, despite this importance, the canopy has been largely neglected by researchers, until recently. Many difficulties in forest canopy research apparently arise from problems related to access. In a survey of 112 canopy researchers, examples of problems cited include: bias in the selection of study species or sampling locations; difficulties in obtaining adequate replication; problems in collecting data in a three-dimensional, complex envi ronment; logistical constraints inmoving between canopy sampling points; and, disturbance, sometimes including interference of the object being studied (i.e., 'demonic intrusion') caused by access. Many of these problems have at least partial solutions. These include: using multiple access techniques to give greater sampling flexibility; identifying appropriate units of replication within the canopy; using ground-operated canopy sampling methods; and, using protocols for unbiased and systematic data collection in three-dimensional sampling space. Designing experimental protocols for work in the canopy requires at the outset the allocation of time and resources for anticipating and overcoming the particular sampling problems associated with the work.
cause and a consequence of significant advances in canopy access techniques (Barker & Sutton 1997).
Introduction A
tree's
(Ronald
a
tree. How
Reagan;
speech,
many
do
you
12 September
need
to
look
at?
1965).
man
(Allen 1996), the crucial role of the canopy in forest atmosphere fluxes (Fitzjarrald & Moore 1995), and its (Bal dominating effect on understory microclimate docchi & Collineau 1994; Barker 1996). However, in reaching sampling points in practical difficulties tall forests or within deep crowns has been a major obstacle in some studies (Schowalter & Ganio 1998).
any
The growth of canopy research during the last two (Moffett & Lowman 1995) has been both a
use
and
of
improved
access
methods
have increased, research opportunities and output have grown (Nadkarni & Parker 1994; Nadkarni & Low
Forest canopies have enormous importance in the overall functioning of forest ecosystems, and have been the focus of a rapid increase in research activity. for conducting canopy research includes Motivation the high species richness associated with the canopy
decades
awareness
As
1995). of
ficulty
Nevertheless, access
as a
many major
researchers
obstacle
regard
to their
dif
research:
40% of researchers in a previous survey (Nadkarni & Parker 1994) regarded access as a 'very important' obstacle to the advancement of science, greater than other
Even
obstacle.
as access
methodology
is im
proved, it seems likely that all methods will continue to have inherent sampling limitations (e.g., Reagan 1995; Barker & Sutton 1997; Bongers 2001). As
problems
of
access
are
resolved,
researchers
to determine what experimental work is possi ble or, more importantly, impossible, using available techniques for canopy access (Lowman & Wittman 1996). To establish the potentials and the limitations need
24 of experimental work in forest canopies, to
evaluate
to
constraints
canopy
it is necessary (Barker
sampling
few publications refer to canopy 1997). Relatively see et issues al. 1993; Koch et al. (but sampling Kapos Baldocchi & Collineau 1994; 1994), however, above ground forest sampling strategies have been receiving increased attention since the mid-1980s (Gr?goire & Valentine
1996; Basson & Bazzaz 1997). The principal constraints to research specifically imposed by limitations in canopy access are mainly problems associated with the choice of site or study species, achieving adequate replication, avoiding dis turbance to the subject being studied, and working in a
three-dimensional
heterogeneous,
this paper, we discuss areas in turn although,
In
environment.
these four possible problem in practice, they tend to be
interdependent.
Rather than attempting to review sampling limita tions throughout the range possible of canopy studies, we focus instead on sampling issues emerging from comments made by 112 practising canopy scientists; many of these (including ourselves) work predomi nantly in plant sciences (68%) and in tropical coun tries (62%; see below); some of the sampling issues raised in the paper reflect this bias. However, many of the problems discussed in this paper are generic and extend beyond tropical plant-based studies. Wherever
we
possible,
cite
from
examples
pub
lished sources to support the points made by the sci entists in our survey. The literature was searched using ,Forestry major databases (Tree? ,CAB? Agr?cola? Abstracts? ), resulting in citations of studies (cf., re views) from 27 peer-reviewed journals. Where no such sources
have
munications.
been After
found,
we
have
all,
our
main
paper is that sampling difficulties in
scientific
papers,
used
in
this
are rarely discussed
because
perhaps
com
personal
contention
the
experimen
to avoid such problems, or tal design was modified because the problems were not recognised. Although our main theme is in suggesting possible weaknesses in canopy
research
due
to access-related
problems,
we
do not identify examples of specific studies which we feel may have been undermined by such problems. In evaluating possible consequences of canopy ac cess on experimental practice, there is a risk of over emphasizing the limitations. Because of this, we have tried whenever possible to suggest possible solutions to apparent limitations, again, based on published ma terial
and
canopy presenting
personal
researchers. more
communications Inevitably, problems
than
with however, solutions.
numerous we
will
be
The aim of this paper is to consider a simple but important question: does the choice or availability of canopy access method affect the science that is being done in the canopy? This question applies to both qualitative and, particularly, quantitative canopy science. The basic premise is that canopy scientists should apply the same rigor to their experimental design as do their terrestrial-based colleagues.
Sampling
A
problems
and solutions:
a survey of
researchers
canopy
survey
was
conducted
among
canopy
researchers
using e-mail addresses mainly from the current listing of the International Canopy Network (2103 Harrison NW, Suite 2612, Olympia, WA 98502-2607, USA) and the list of delegates at a European Science Foun dation conference on Tropical Canopy Research (Ox ford, UK; 12-16 December 1998). We cannot be sure how representative the respondents were of the wider community of canopy scientists, especially as those who
responded
were
self-selected.
However,
we
can
at least conclude that those surveyed are interested or concerned in sampling issues, since they responded to requests for information. A limitation of the survey is that only networked scientists were contacted and, of these, 28% responded. Nonetheless, the numerous were issues raised canopy sampling frequently raised more one than of the researchers independently by who responded, and were often also supported by pub lished material. For these reasons, we believe that responses in the survey are likely to be broadly rep resentative of opinions held by active scientists who have considered possible canopy access influences on sampling. The number of respondents to the survey was intermediate in size between previous surveys of canopy scientists by Stork & Best (1994) and by Nadkarni & Parker (1994); both the previous studies focused on other issues in canopy research. The survey (further details of which may be ob tained from the corresponding author) was intended to elicit information without preempting responses. We asked researchers to choose which subject area(s) they worked in (from an initial list of 11 choices; Table 1), which canopy access method(s) they use (from an initial list of 11 alternatives; Table 2), and which coun try/countries they conduct canopy research in. The remainder of the survey consisted of the four questions (with three possible responses) shown in the captions for Figures 1-4. For each of these questions, we asked
25 1. Distribution of canopy researchers surveyed across subject areas, with proportion of in study sites in tropical or temperate countries. The number of canopy researchers working as is the total number of countries each of the subject areas listed in the survey is presented, in each subject area. Sixty-seven listed by researchers working percent of researchers complet ing the survey listed more than one subject area and most listed more than one country. Work
Table
conducted in Brazil was assumed to be tropical and work conducted in the USA was assumed to be temperate. As alternatives to the 11 subject areas listed in the questionnaire, subjects marked * were suggested by some researchers. area
Subject
Number
of
researchers
Plant ecophysiology
35
Plant ecology
32
Biodiversity
30
Animal
24
ecology fluxes
Canopy-atmosphere Nutrient
24
cycling
19
Micrometeorology
17
Herbivory
16
Plant Forest
systematics
9
structure*
9
Pollination/fruit
development
Animal
behaviour
Animal
systematics*
Frugivory/seed Population All
table
Contingency relative
for various
gories
were the
received countries
234
listed
to compare
used
observations
across
groupings.
Responses
to the
from 112 canopy researchers; in which
ical, 40% temperate sites
was
in temperate
the
respondents
work
cate survey
60% of are
trop
(Table 1). The number of study versus
tropical
countries
var
ied by subject area (x2 tests, p < 0.001, using the eight subject areas listed most frequently in the sur vey). For most individual subject areas, the proportion of work being done in tropical versus temperate areas was not different from the overall division between tropical
and
temperate
work.
However,
tropical
temperate
countries
countries
73 48 75 69 23 42 50 60 91 40 92 86
27 52 25 31 77 58 50 40 9 60 8 14
60
40
Total number of countries
not
surpris
studies proportionally more ingly, for biodiversity work was being done in tropical rather than temper ate countries (p < 0.03). In contrast, proportionally more canopy atmosphere flux work was being done in temperate areas (p < 0.001). The relative number of
listed
52 58 59 48 35 26 34 25 10 23 14 12 1 1
1
areas combined
analysis
sites in
1
genetics*
of
frequency
% Study
sites in
1
dispersal*
respondents reporting 'some limitations' or 'serious limitations' to provide further information including, if possible, means by which difficulties are overcome. the
% Study
None
listed
398
plant ecophysiologists conducting work in the tropics was only marginally greater (p = 0.07) than expected. No tests were conducted for subject areas with fewer than
10 researchers.
A range of canopy access methods are used by the respondents to this survey (Table 2). A high proportion (66%) of canopy researchers use a combination of ac cess methods (see also Nadkarni & Parker 1994). The most common combination of methods involved the use of rope (either in single rope technique (SRT) or arborist methods; see Barker 1997) and ground-based methods,
Lowman
consistent
with
& Bouricius
previous
1995). The
observations
(e.g.,
relative frequency of canopy work in tropical/temperate sites varied with access method (y} = 20.1, df = 8, p = 0.01; using the eight access methods listed most frequently in the survey). Ropes were used in tropical sites more often than expected (p = 0.03), and scaffolding was used in = temperate sites more often than expected (p 0.02). to the indicated that in survey Responses flexibility the choice of canopy access methods is an important
26 Table 2. Distribution
of canopy researchers with propor surveyed across access methods, tion of study sites in tropical or temperate countries. Presented are the number of canopy researchers either in combination with another surveyed using different access methods, or as the main access method. As alternatives to the 11 methods listed in the method, * access methods marked were suggested by some researchers. questionnaire, Access
method
All
Main
users
access
Ground
65
Rope
46
Tower/walkway
40
Ladder
24
Crane
20 16
Scaffolding Remote
14
sensing
Cherry
/ hydraulic
picker
lift
9
Spikes
5
Tree grippers2 Treefall / felling*
4
climbers
Dirigible
3 '*
Free climbing Local
users
3
3'*
/ canopy
2 raft
1 1
Helicopter* Boat4,t4,*
1
236
Totals includes
of increasing or
advantages are
niques
sampling capability. The general of
disadvantages
described
elsewhere
access
different
Lowman
(e.g.,
tech et
al.
1993; Lowman & Moffett 1995; Barker 1997; Barker & Sutton 1997). A comparison of most frequently used canopy ac cess methods in relation to the most frequently cited areas that the relative use of the dif indicated subject ferent methods varies by subject area (x2 = 40.5, df = 20, p = 0.004; animal ecology was not included in the analysis) (Table 3). The frequency of respon dents using ropes was variable across the subject areas; ropes
were
used
a greater
to
extent
researchers
by
working in biodiversity and animal ecology, compared with other subject areas. Ropes presumably offer rapid and flexible access for sampling in these sorts of
studies.
In contrast,
researchers
studying
canopy
appear to use atmosphere flux or plant ecophysiology ropes less frequently than other groups; we assume that
this
is because
these
workers
mostly
use,
respec
% Study
sites in
sites in
number of
tropical
temperate
countries
countries
countries
listed
Total
22 21 20 5 8 5 0 3 1 0 1 2 0 1 1 0
46 64 43 60 56 26 33 46 77 86 75 83 75 100 Na Na
54 36 57 40 44 74 66 54 23 14 25 17 25 0 Na Na
None
90
51
49
452
binoculars, hemispherical pole-pruners, tree bicycle'. 2'Swiss 3 With little or no specialised climbing equipment. In periodically flooded forest.
means
% Study
photography,
tively,
105 84 76 40 39 27 21 13 13 7
radio tracking,
automated
fogging.
instruments
bulky or delicate not
listed
installed
for which
equipment
on
or
towers,
rope access
is
suitable. Choice
ence, research.
of
and be Science
canopy
access
influenced usually
by, begins
can
techniques
the objectives with
a
question
influ
of
the or,
more
formally, a hypothesis. In canopy science, there are important, unresolved hypotheses awaiting atten tion from researchers (e.g. Smith 1973). However, in
canopy research detailed experimental plans cannot be made until a decision has been taken on which canopy access methods are appropriate and available. Other factors affecting choice of access method will also be referred to in the following sections.
27 of canopy researchers in each of five most popular subject areas using the five Table 3. Distribution of total researchers working in each subject area, using the most popular access methods. Percentage listed parenthetically). listed access method (actual number of researchers by access method Subject
area
or
Tower
Ladder
Crane
Rope
Plant ecophysiology
access
14(10) 13 (8)
Biodiversity
fluxes
Canopy-atmosphere Animal All
Effects
6 (3) 12 (5)
ecology
others
of access method
8(8) 12(9) 8 (5) 11(6) 5 (2) 13(29)
21(20)
Plant ecology
15
(35)
on choice of study site or
location
of
access
is often
systems
non-random
and opportunistic. Sampling may also be arbitrary (referred to by Lowman (1997) as 'reach-and-grab'), possibly being restricted to accessible parts of a crown (Schowalter & Ganio 1999). Potential sample material may therefore be beyond reach (Elton 1973). Positions of sampling points may in number,
or
be unrepresentative,
inconvenient.
simply
These
limited
constraints,
are often unavoidable, appear to apply to most canopy access methods. We will describe sampling is sues associated with low- or high-tech access methods
which
(sensu Barker & Sutton are often
used
Low-tech
canopy
access
Low-tech
methods
methods
1997) separately
though the
in combination.
methods
such
as bole-climbing,
rope
climb
ing and ground-based methods are generally highly mobile so, in theory at least, should not compel the researcher
in a particular
to operate
forest
(or part
of
forest), or to study a limited range of species. Sur vey results provide some support for this assertion for rope access (Figure 1), but less so for ladders. A high proportion of researchers (41% of those in our survey) use rope access methods, but climbing to trees limited is with con by ropes large, healthy venient
branches,
and
access
to
the
outer
canopy
10(9) 21(15) 32 (20) 9(5) 33 (14) 18(41)
15(14) 7(5) 8(5) 15(8) 2(1) 6(14)
methods
20(19) 27 (20) 26(16) 26(14) 29(12) 24(55)
26(25) 19 (14) 13(8) 33(18) 19(8) 24(54)
access methods which require support from trees, size of tree is an issue; 'intermediate' sizes may be too tall to reach with ladders, but too small to support climb
study species The
All other
Ground
walkway
is
often limited (Nadkarni & Longino 1990; Longman et al. 1993; Moffett & Lowman 1995). However, there are techniques for extending the horizontal range of 1981; sampling from ropes (e.g., Perry & Williams Whiteacre 1981; Dial & Tobin 1994; Barker 1997). Vertical sampling range can be extended using pole pruners (Mori 1995; Wieringa 1996). With low-tech
(E. Braker, pers. comm.). The ing by other methods smaller size of mature trees in secondary
generally
can
forest pers.
limit
access
safe
(F. van Dunne,
ropes
using
comm.).
though versatile
Ladders,
studies
preclude
tree
within
and fairly mobile, crowns.
often tree
Sectional
climbing ladders are fairly bulky and heavy (e.g., each 3-m section weighing 5-8 kg) but have been used in Sarawak to access tops of trees 60-70 m, though portage of the sections from nearest road is a limit ing factor (K. Reynolds, pers. comm.). Free-standing (guyed) ladders have been used in combination with to reach crowns up to 20 m (Morris pole-pruners 1955). Ground-based techniques (see Table 2 for exam of these) provide complete two-dimensional mo ples are often used as a supplement to methods and bility, access
direct
giving searchers
(58%
to
in our
pling of the canopy access
method.
tions
from
the survey)
canopy.
also
re
Many
use
sam
remote
from the ground as their main
Computer
ground-based
forest
allows
modelling
estima
validated
measurements,
by
some direct sampling in the canopy (M. Hanus, pers. comm.). However, many (68%) respondents using ground-based methods reported constraints on choice of study species (Figure 1). The main problem seems to be in sampling or observing crowns of tall trees in forests (e.g., Shaw & Bergstrom 1997). multi-layered However,
ground
observations
topography allows viewing (M.
Shanahan,
pers.
comm.).
are
easier
if
the
site
crowns from nearby ridges In cases
where
actual
sampling (cf., observation) is from the ground, there will be an influence on which trees (species or ages)
28 100
Scaffolding
Some effect
Serious effect
Serious effect
No effect
Some effect
No effect
Serious effect
Some effect
No effect
on choice of study location or study species. The corresponding in the survey was: do 1. Effects of canopy access method question are were on or location included in studies? limitations which forest forest your canopy access problems type Respondents impose species, some limitations; no effect. Results are only for researchers serious limitations; asked to choose one only of the three alternative responses: are shown. Sample sizes (number of respondents) using one of the techniques shown here as their main (possibly only) access method.
Figure
the use of light aluminium including some walkways, rather than traditional heavy construction materials al
are accessible, though the experimental not require higher access (e.g., Meinzer design might etal. 1995). or lifeforms
In extreme
access
cases,
access
ground-based
northern boreal forests may assisted by, increased snow the year (Esseen & Renhorn et al. 1993). In periodically provided by boat (S. Filoso, seasonal
such
to the
For in
canopy
depend on, or at least be depth at certain times of 1996; Sorrensen-Cothern flooded forest, access is pers. comm.). Whether
constrain
phenomena
using
seasons.
lower
lows
low
sampling
regimes
is subject dependent.
presumably
access
canopy
High-tech
canopy
to particular
is limited
tech methods example,
to the
are high-tech access systems (e.g., hydraulic lifts, scaffolding, booms) that can be moved to differ ent locations within forests. In the case of scaffolding, at least, there are indications that there is little or no effect on choice of study site or study species (Fig
There
ure
depend cess at
with pers. tected
these
1). However, on
access.
road
some
or
sites,
are
systems This
heavy
of
sites,
and
usually ac
restricts
presumably
parts
including
those
soft substrate (Inoue et al. 1995; E. Middleton, comm.), areas.
steep In
the
or
unstable
case
of
in forest-edge As
terrain,
smaller
static
or
in pro systems,
structures
to be
taken
to more
remote
with
studies. some
low-tech
methods,
there
are
upper
height limits thatmay exclude some studies using mo bile towers and lifts (e.g., ca. 12 m; Morris 1955; 1988) and scaffolding towers (35 m; M. McCarthy Ryan,
methods
access
parts of forests (Inoue et al. 1995), which presumably allows a greater choice of potential study locations. Hydraulic lifts (cherry pickers) often cannot be moved away from roads, although they can be very effective
pers.
comm.).
However,
these
systems
have
an
advantage over static towers in allowing the height of sampling positions to be adjusted over time to keep up with height of fast-growing trees (e.g., in plantations) (J. Chambers, pers. comm.). Tall scaffolding can also support platforms at a range of heights, providing ac cess throughout much of the forest profile (Bond et al. 1999). in how sampling problems There are differences are dealt with by researchers using static versus dy namic high-tech methods. Static systems such as tow and platforms occupy fixed locations ers, walkways, within forests. Towers are inevitably located in canopy gaps (Parker et al. 1992). The location of walkways and platforms is often determined by the presence
29 of large, healthy support trees (Reynolds & Crossley 1995) and is dependent on the structural integrity of the forest (Moffett & Lowman 1995). Other factors which influence the location of towers and walkways include topography and also the demands of tourism, since
of
many
these
large,
expensive
are
structures
built wholly or partly for use by forest visitors (e.g., Muul & Lim 1970; Sutton 2001). Once installed, static systems provide access to a limited number of trees (Nadkarni & Parker 1994) and (by definition) cannot be relocated to other parts of the forest, although they can be expanded laterally (Inoue et al. 1995; Low man & Bouricius 1995). Further, the vertical sampling position of many access platforms is restricted to a particular vertical zone of the forest profile, neglect ing some (e.g., lower) parts (e.g., Mori 1995). Given that some species are distributed unevenly through out the vertical forest profile, sampling at a restricted range of heights may a problem for some types of studies. Since the location of sampling points from access facilities will not be random and (for tree-based studies) may restrict access to target or representative species, it is possible that sampling will be biased, or that some intended
in fact be
studies may
'ecological'
Many
in the
researchers as
their main
survey
access
who
method
use do
towers not
and a
report
strong effect on their selection of study site or study species (Figure 1). One explanation for this is that ex periments
are
'around'
planned
what
species
can
be
reached from the sampling point. Another possibil the limitations of fixed sampling ity for minimising use is the of additional access methods (e.g., points by rope,
pole-pruners,
the main
tower
temporary or walkway.
walkways) The
precise
as well
as
dimensions
of the footprint (sampling area) of micrometeorolog ical towers may be unknown (Aber et al. 1996), but the tree species composition within the footprint are likely to influence biogenic fluxes and, during dry pe riods, water fluxes from the canopy (F.Mowry, pers. comm.); towers should presumably be positioned to include 'representative' trees within their footprints. Although dynamic within their area of operation (typically ca. 1 ha), cranes are confined to fixed sites forests resulting in limitations to choice of or species (see Figure 1). Researchers using site study cranes adjust their experimental designs to accommo date sites or species which are within reach of the
within
gondola
(e.g.,
planning other
cranes
reach
the
F. Meinzer,
pers.
their field operations
researchers'
priorities.
comm.),
around
Researchers
as well
the needs who
work
as
of
some
in
inner
cases of
parts
use
also
tree crowns,
access
rope
where
to
the gondola
cannot penetrate (Gilbert 1995). Further, a new gener ation of cranes have a much increased sampling foot print: examples include the Surumoni (Venezuela) and Wind River (USA) cranes (see Sutton 2001; Szarzyn ski & Anhuf 2001). Other highly flexible high tech systems include COPAS, which operates using a fixed cable network (Sutton 2001). There are a range of high-tech techniques (e.g., di rigibles, helicopters, balloons, remote sensing) which allow
sampling the canopy from above. Of these, the dirigible technique allows both remote and direct canopy sampling (Lowman et al. 1993) and can also be used to deposit a 'canopy raft' onto the canopy. In researchers
addition,
the
using
can
raft
use
tech
rope
niques or pulleys to increase the vertical range of their 1995). Choice of study site sampling (e.g., Cosson and study species (of trees) will be strongly influenced by the requirements of this technique. For example, the canopy raft needs a structurally cohesive forest for support, and its placement is affected by the presence of ?mergents and gaps. Also, the location and duration of sampling from the raftmay be affected by the differ ent
'autecological'.
walkways
from
of other
needs
researchers.
this
However,
versatile
system provides invaluable access to the outer canopy, which many other techniques do not allow (Lowman etal. 1993). in this group,
Finally not
any,
impose
or study species,
on
constraints,
work.
Remote
do site
study
from
though they require validation
or ground-based
canopy-
methods
above-canopy
or many
may
sensing
need simultaneous ground truthing at the same spatial scale, and it is difficult to get the required resolution (e.g., 10-30 m) by ground sampling (S. Bohlman, pers.
Aerial
comm).
foliation) nique
appears
when
checked
against
General problems
estimating
de
tech
observa
ground-based
tions (MacLean & MacKinnon
of
(e.g.,
sketch-mapping
to be a reliable 1996).
relating to study site of species
Some additional general points spontaneously emerged from this part of the survey, in relation to possible canopy access problems on study species or forest type or
forest
location.
minimise access
Firstly,
many
researchers
canopy
such constraints by using a combination techniques.
However,
choice
of
access
of
method
is itself limited. Cost is a major factor in determin are actually used. Other factors ing what methods (e.g.,
safety,
convenience)
were
rarely
mentioned.
30 are well
researchers
Secondly,
aware
of
in
potential
fluences of access method on experimental designs. In some cases, while choice of study species/site may not be
access
affected,
may
influence
strongly
tions can be asked (Bassow & Bazzaz
what
1997; J. Read,
comm.).
pers.
Effects
on replication
access methods,
and
can
priately,
have
two
on
effects
Firstly, access methods may cate
measurements
or used
if chosen
inappro studies.
quantitative
limit the number of repli can
which
be
made
Zotz
(e.g.,
& Winter
and 1996). In the highly heterogeneous in complex canopy environment, especially tropical forests, lack of replication may mean that spatial or temporal variability in the environment is not repre sented in the data (Lowman et al., 1993; Lowman 1997). access
Secondly,
may
problems
result
in
statis
tical comparisons being made between groups of 'replicates' that are not truly independent, which is pseudoreplication (Hurlbert 1984). Sutton (2001) believes that pseudoreplication has 'claimed many in
victims'
canopy
studies.
However,
the
point
at
is highly replication becomes pseudoreplication subject-dependent. Put another way, the unit of repli cation depends on the type of study being conducted ecol (see Bongers 2001). For plant physiological ogy or invertebrate ecology studies, typical replicates
which
are
trees,
studies
while use
plant
replicates
ecology at the
canopy,
or
This
be
representative
even reached,
easily
can
samples
some
is because
ac
of
However,
1993). can
sub-canopy
sufficient,
obtaining
because
mainly et al.
(Lowman
the canopy
is difficult when
replication
access
a
be ef
techniques
fectively provide only one fixed sampling position (Schowalter 1995), either within a tree or within the forest as a whole. Aside from replication, working from a fixed position is a particular problem when us
pseudoreplication Canopy
sampling cess constraints
problem.
of access method
outer
the
when
ques
sufficient
Achieving
or
micrometeorological stand or community
ing destructive sampling because the removal or study material can limit (at least temporarily) subsequent 1995) and can also sampling (Reynolds & Crossley alter local microclimate Several published a
single
leaves
Arthropod studies involve a range of possible sam pling methods, which includes tree-level approaches such as fogging, where the orgins of sample mate rial within the forest profile are not usually known, although yields per unit effort are comparatively
In
such
cases
'dendrocentric'
et al. 1989), within-tree
Lieberman and
branches
been
have
(sensu
such as
samples as
used
on
replicates.
truly independent samples can be collected a within and depends on single tree is questionable, the type of study being conducted. For example, indi vidual branches can sometimes be regarded as being
Whether
autonomous for water relations (Sprugel et al. 1991) or carbon economy or herbivory (Watson & Casper leaves taken from different 1984). In such cases, branches can be treated as independent and not as (e.g., Barker & Booth 1996). How pseudoreplicates ever, the status of leaves as independent functioning units
is debatable
(Caldwell
et al.
1986; Leverenz
1988). In many
ecological
the stand or community are
trees level.
tree.
and microhabitats. canopy studies are based
only
studies,
In
sub-samples.
occurs
replication
cases
at
case individual
level, inwhich
where
samples
taken from a single tree or forest stand are not truly has independent in space or time, pseudoreplication occurred (see Hurlbert 1984), and the sample size is one.
effectively
Within-tree ies.
For
example,
sampling
is common are
researchers
in canopy
often
stud in
interested
1995; Schowalter 1995). high (Reynolds & Crossley Branch-based sampling (unlike fogging and inter ception traps) is targetted and allows a standardised expression of arthropod abundance to be calculated
understanding variability in tree crowns. Such sam pling is repeated at a tree or stand level to give replication. Since canopies are known to be highly heterogeneous (e.g., Harper 1989), it is important to
(numbers of arthropods per unit of associated plant material), which permits comparison with other stud ies (Schowalter & Ganio 1998) at least for sessile
reduce
species (Schowalter 1995). Ironically, sampling capa bility of canopy arthropods has now outpaced labora tory processing of material, perhaps by a factor of at least four times (Erwin 1995).
or
remove
bias
in within-tree
sampling.
Re
searchers have developed protocols for this, including randomized branch sampling to estimate total leaf area, biomass, or insect egg or larval populations (see Gr?goire et al. 1995; Zandt 1994). Another example is the use of paired sampling, for example of 'sun' and 'shade'
branches,
because
such
sampling
allows
for
31 100 r
Ladder
Tower/walkway
Scaffolding
n=5
n=5
75 h 50 25
E 0 ** ?ioo o
1I...II.. Ground
Crane
Rope
n=22
n=8
a75 o
.Il
Serious effect
Some effect
No effect
II.
Serious effect
Some effect
il
Serious effect
No effect
Some effect
No effect
Figure 2. Effects of canopy access method on replication. The corresponding question in the survey was: do canopy number of independent replicates you include in your studies? For further details, refer to caption for Figure 1.
within crown variability and thus gives greater power in statistical tests (Brooks et al. 1996). We believe that canopy researchers are generally well-aware of the problems of obtaining a sufficient number of independent replicates from fixed sam pling points. In the survey reported here, effects of access method on sampling are reported particularly by
researchers
tures,
whether
using static
methods (tower,
bile (crane, scaffolding) Furthermore,
the
involving walkway)
even
struc mo
the forest (Figure 2).
within structure
canopy
large or
can
itself
obstruct
potential sampling positions (Hollinger 1989). Sam pling repeatedly from a tower platform or walkway cannot provide information on variation on a within forest
scale.
for example stand-scale
Variation
also
for herbivory replication
occurs
(Lowman
using
forest
among
multiple
stands,
would
need a huge budget (E. Miller, pers. comm.). For a walkway and platform system providing access to ca. 10 canopy trees and 25 undersory trees in Belize, Low man & Bouricius (1995) report a cost (in 1994) of about US $32000. Cranes and scaffolding have a capability to access several trees, yet a high proportion (58, 80%) of re searchers using these methods on
replication.
Cranes
report 'serious effects'
in particular
have
huge
sam
1996); for example, pling capability (Zotz & Winter access of one crane in Panama was 8000 m2 on the up
limit the
problems
per canopy surface, 28 000 m3 of forest volume, or 140 individual trees (Allen 1996). Thus, it could be argued that replication is only limited by time, which is itself constrained by budgets (W.Winner, pers. comm.). However, the relative flexibility that cranes or mov able scaffolding allow is often only within part of a single forest stand. Even within a tract of forest, there are logistical problems associated with cranes and scaffolding that can limit the number of trees can if the study is fo which be reached, especially on
cusing
a
single
are generally (F. Meinzer,
be
used
as
or no
(R. Oren,
in physiological
functional
of
rope
access
groups
may
comm.).
pers.
in the survey mainly
effect
studies
abundant species
However,
within
species replicates
Researchers some
to the most
comm.).
pers.
tree
Crane-based
species.
restricted
measurements,
1997). However, towers
access
reported either
on obtaining
adequate
replication. Access by rope at any one time is usually limited to a single tree. However, access and therefore independent sampling can be increased by climbing a succession
of
trees
over
time.
since
Alternatively,
rope
access
is a relatively inexpensive technique, multiple sets of rope equipment can be used to access several trees simultaneously by a group of researchers work ing together. Such temporal or spatial replication can
of
course
munity.
include Achieving
be mainly
more
than
replication
one
forest
using
limited by researchers'
stand rope
or com
access
may
energy and time (E.
32 100
Scaffolding
Serious effect
No effect
Some effect
Serious effect
Some effect
Serious effect
No effect
No effect
Some effect
access
question in the survey was: do canopy Figure 3. Effects of canopy access method on disturbance. The corresponding refer to caption for Figure 1. further are For to which the disturbance details, you measuring/observing? any subject
Olson,
comm.).
pers. is
time
as
seen
a
of sufficient
Availability
constraint
by
field
researchers
canopy
(Nadkarni & Parker 1994) and, for canopy arthro pod studies, the time required for processing sampled material needs to be allowed for (Erwin 1995). Even
ground-based
methods
are
as hav
regarded
mote
sampling of the upper canopy (e.g., by shotgun) from the ground may be restricted for similar reasons. can
canopy
the
reduce
researchers
risk
of
in their studies? A common bias and pseudoreplication to increase is sampling flexibility by using approach more
than
respondents
one
access to
the
technique. survey
who
For use
example, or crane
in a more
extensive
system
(e.g.,
and increased
replication
cause
(R.
comm.).
pers.
An approach which appears to be used increasingly ismodelling, making extrapolations from limited sam are pling in the canopy. Actual canopy measurements often
or validate
to calibrate
then be applied
verified
(E. Miller,
any model,
that
can
to a range of sites and further
pers.
comm).
survey comment on their though many indicate than access per se which the direct or indirect ef sampling, it is important to develop appropriate an experimental design for each study. Also, sampling strategy should be clearly ex plained in themethods section of papers (Barker 1997;
Several researchers in the desire to increase replication, that it is time and costs rather are limiting factors. Whatever fects are of canopy access on
B. Kloeppel
comm.).
pers.
several
Disturbance
and
intrusion'
'demonic
ground
based methods as their main means of canopy access also use ropes. Sampling resolution with any single access technique can also be increased spatially by an investment
shared dataseis
necessary
re ing some effect on sampling by about 41% of searchers using this method (see Figure 2). For exam ple, intervening vegetation (especially in tropical rain forests) can limit the number or quality of observations made from the ground in both plant and animal studies (Gillesberg & Carey 1991; Fintoura 1995; Fisher & Araujo 1995; Kaplin et al. 1998; Leite et al. 1996). Re
How
lowing Fournier,
problems
for walk
1995) or multiple access ways; Lowman & Bouricius units (e.g., for rope methods; Lowman & Bouricius 1995). Another approach is to develop a common experimental design with other research groups, al
Canopy
access
or
structures
activities
turbance in the canopy. Although impose
constraints
on
the
scope
can
cause
dis
canopy access may and
quality
of
sam
pling, such limitations have generally only recently been explicitly discussed by researchers (Moffett & Lowman 1995, Barker 1997). 'Demonic intrusion' here refers to the specific effects of access activities on the variable being sam
33 In the survey, a majority (98%) pled or measured. of canopy researchers felt that their primary access method
caused
only
some
or
disturbance,
no
distur
or observed bance, to the subject being measured access meth 3 shows this trend for six of the (Figure can also But disturbance, ods). including damage, affect parts of the canopy not being studied. For exam ple, branches broken by a crane's gondola or epiphytes dislodged by ropes may not be the subject of a par ticular study. However, the gradual degradation by access activities of a forest which is being intensively researched may have a significant impact on future at
research
the
same
This
site.
a
be
may
particu
lar problem in forests which are fragile (i.e., easily and/or irreversibly degraded) or in conservation areas, where the movement of heavy or bulky canopy access equipment through the forest is restricted. A further problem of demonic intrusion is that the quality of data obtained may differ according to the access
method
being
For
used.
the
example,
verti
a forest may be from a tower or
cal distribution
of irradiance within differ considerably when measured from a crane's gondola (see Chazdon
et al. 1996). in comparing
Such discrepancies introduce problems results among studies using different sampling proto cols (e.g., Daw et al. 1998), or using different access techniques.
of access-related
Examples
disturbance
Disturbance and accidental damage to plants and ani mals by climbing structures or activities is a concern include: spikes among many researchers. Examples trees to fatal (Donahue & causing potentially damage Wood 1995; Mori 1995); carrying ladders, or mov ing a man-lift, through forests causing disturbance to understory
(B.
vegetation
Middleton,
pers.
lichens
(W. Denison,
causing
nest
canopy
crane
comm.);
abandonment movements
pers.
Lohr,
rope
comm.); (W. Ritchie, temporally
abrading rope
researchers imise
often
or avoid
have
formulated
access-related
to min
protocols and
damage
disturbance.
For example, avoiding physiological measurements on branches that have been in contact with an access tower; periodically moving scaffolding to avoid sam pers. comm.); pling 'degraded' areas (B. Kloeppel, placing towers carefully to avoid them being hit by branches
in wind
moving
(P. Hanson,
pers.
comm.);
avoiding during gas exchange measure ments by turning off the engine of an aerial lift (Bas sow & Bazzaz 1997); avoiding rope climbing at dawn interference
or
dusk,
comm.);
when
birds
observing
most nesting
active
(K. Nelson,
behaviour
with
pers. a remote
on an adjacent tree (W. Ritchie, pers. comm.); reducing disturbance by re peated climbs by using pulley systems, allowing small mammal traps to be lowered for regular inspection controlled
video camera mounted
1996; Vieira 1998); reduc (e.g., Taylor & Lowman near the base of a crane to established ing disturbance paths
or
boardwalks
(M.
Ryan,
pers.
comm.);
and,
damage to the undersory during walkway minimising construction (Lowman & Bouricius 1995). More generally, the risk of disturbance, including possible demonic intrusion, can be reduced by limit ing the numbers of researchers entering study sites, flow among project ensuring good communication participants (R. Fournier, pers. comm.), by periodi cally relocating the sampling site (S. Thomas, pers. comm.) and by restricting intensive destructive sam . pling in sensitive habitats (C. Ozanne, pers comm.). For all studies, data should be rejected if evidence of disturbance
is obvious
(J. Massheder,
pers.
comm.).
E.
comm.;
pers.
movements
So, what are the solutions to such problems? Though not routinely referred to in scientific pub it is clear from our survey that canopy lications,
Logistics
and hyperspace
climbing
pers. scaring
comm.); away
larger birds (D. Shaw, pers. comm.); canopy walkways interfering with malaise trapping (Preisser et al. 1998); canopy walkways influencing the movements of arbo real animals (Perry & Williams 1981; but see Lowman & Bouricius 1995); climbing and branch sampling insects (Morris 1955); and, large access disturbing structures affecting microclimate (Parker et al. 1992; Koch et al. 1994; Moffett & Lowman 1995; Sutton 2001).
Stork & Best (1994) suggested that lack of spatial replication is a major problem in nearly all canopy research. One explanation for this is that there are a number of problems in working in three-dimensional (3-D) space which affect the logistics of sampling (Nadkarni & Parker 1994), though such problems tend to be subject-specific. Planning sampling regimes tree crowns needs to take into account the spa tial variability of the parameter being measured. Such variability is, for example, large in studies of herbivory (Lowman 1997), arthropod distribution (Schowalter & Ganio 1998) and stomatal activity (Elias 1979). If within
34 variables are statistically between
the upper
and
different
lower
crown,
(or at least distinct) sampling
must
al
low for this; in practice, more sampling effort might be to ensure that upper crown data are collected
needed
(Schowalter & Ganio difficult to reach. Sampling The
1998), since this region is more
in complex, 3-D space
complexity
of
3-D
environments
can make
col
lecting data, and representing results, difficult (see Lowman 1997; Bongers 2001), including for ground level observations (Leite et al. 1996). Actual sampling within the 3-D matrix causes particular problems. For example, the distribution of leaves within a crown is difficult tomeasure (Russell els are now being developed (e.g., Pearcy. & Valladares Another approach is to
et al. 1989), though mod for describing leaf arrays 1999). use manipulated
or simu
lated canopy structures. Examples include the instal lation of branches (Renhorn et al. 1997), living tree leaves (Rowe & Potter 1996) or bryophytes (Clark et al. 1998) at particular positions within the forest structure, or simulated canopy branches (Schlesinger et al. 1993) or trees (Hubert & Messier 1996), or ac tual branches (Parrish 1995) in laboratory conditions. An advantage of such approaches is presumably to simplify the 3-D canopy by isolating and defining the variable under investigation. Various protocols have been developed for defin ing sampling points in 3-D canopy space (e.g., Ford & Newbould 1989; Castellanos et al. 1971; Hollinger also require tech 1992; Sumida 1995). Researchers data collected for and representing niques analysing from 3-D sampling (Richards 1983; Popma et al. 1988; Nadkarni & Parker 1994; Barker 1997). The trend in increased efficiency and lower continuing costs of computing processing capability will make the analysis of such data more feasible (Weishampel et al. 1996; see Bongers 2001). Another important consequence of working in 3-D space is that moving between sampling points often introduces a temporal dimension. Canopy sampling may thus occur in a four-dimensional hyperspace. This is likely to be a particular problem for studies involv ing transient changes in the object being measured or observed.
For
example,
forest
canopy
microclimate
typically show large temporal fluctuations Baldocchi & Collineau 1994; Barker 1995) (e.g., which can occur over small spatial scales (Chazdon et al. 1988). In real-time sampling, such fluctuations variables
could be a problem given the added time required to move around in the canopy (Kapos et al. 1993). A result of this is that canopy measurements sometimes lack temporal resolution (Fitzjarrald & Moore 1995). limitations of the canopy may sampling Temporal affect what type of research can be undertaken. For example, samples (e.g., flowering parts) collecting from trees takes much more time than collecting from trees may be under shrubs or herbs, consequently some in represented systematic studies (J.Wieringa, comm.).
pers.
Logistical with
and
problems access
particular
some
solutions
associated
methods
The type of canopy access method has implications for the frequency and duration of sampling, and the type of equipment being used. For example, rope or bole climbing techniques may be unsuitable for use with heavy or delicate equipment, and when the researcher needs to sample for long periods in the canopy. Bole climbing methods inevitably restrict sampling in the outer crown area (Hietz 1997). Even when access are used in combination, certain parts of the canopy may be difficult or impossible to reach, result
methods
in a possible
ing
of
under-representation
some
sample
types (e.g., Wright et al. 1997). in our survey indicated that problems Responses associated with the logistics of sampling occur with all main canopy access methods, though relatively few researchers (< 20%) in our survey felt that access im posed 'serious' effects (Figure 4); canopy cranes have large sampling capability (see above). Researchers can repeatedly revisit a sampling location, and can move around in the canopy with heavy or bulky equipment. However, temporal sampling may be constrained by the high costs involved (Nadkarni & Parker 1994; M. shared
and
comm.)
pers.
Ryan,
because
such
facilities
are
researchers.
among
Studies that involve climbing by the researcher are be likely to impose time limitations on movements tween
sampling
events.
This
may
account
for many
reported by users of ladder, scaffolding and rope systems tower/walkway, on sampling were constraints (Figure 4). Logistical
of
less
the logistical
evident
among
constraints
researchers
using
ladders
and
scaf
folding. These methods are often used for sampling at relatively low heights. Furthermore, the equipment can be moved or duplicated to allow more of the forest area
to be
included
(R. Teskey,
pers.
comm.).
35 100
Ladder
Tower/walkway n=20
Scaffoldingn=5
n=5
75 h
.Il.11.11 100
Io
Ground
Crane
Rope
O a o
n=8
n=22
75
? 50 25 Serious effect
No effect
Some effect
Serious effect
Serious effect
No effect
Some effect
No effect
Some effect
question in the survey was: do canopy access Figure 4. Effects of canopy access method on logistics. The corresponding or can For further details, refer to caption for Figure 1. or observations make in time? number of measurements space you
Rope access is commonly used by canopy re searchers (Nadkarni & Parker 1994; Lowman & Bouricius 1995; Table 2), but for some studies (and in tall forests) this method may impose especially substantial logistical constraints on sampling. For ex ample, ropes do not allow sampling access throughout tree crowns (e.g., Hadwen et al. 1998). It is tiring to climb trees, and this limits the and time-consuming number of trees that can sampled per day (L. Risley, pers. comm.); in cases where extensive (e.g. diurnal) is being
sampling
conducted,
access
rope
may
only
allow sampling from one tree per day (e.g., Barker & P?rez-Salicrup, 2000). However, sampling can be increased by the use of extra personnel during periods of intensive fieldwork (Lowman & Bouricius 1995; D. Coxson,
pers.
trees with sampling using
rope
comm.).
The
for
access
involves
time-consuming
sample
trees,
using
changes
access,
can
be
pose
a
temporal
methods
for
constraint
reason for this is that moving
on
canopy
access
measurements.
1996) which needs to be factored in to experimental protocols. Some ground-based sampling is dependent on suitable weather conditions, such as lack of wind for fogging (H. Recher, pers. comm.). Similarly, the time of day in which hemispherical photos can be is
taken
limited
D canopy
(R. Hall,
pers.
3
However,
comm.).
space can still be sampled effectively
the ground,
microclimate
for
instance
by
using
a balloon
from
to measure
(Parker et al. 1996).
can
Conclusions
im
consensus
emerging
among
re
canopy
searchers that gaining access to the upper part of forests is not the only practical difficulty to be over come in canopy research (Nadkarni & Parker 1994). to be it is necessary To conduct rigorous science, aware of access-related effects on the quantity and quality of sampling. In
One
through ground vege
is an
There a
highly variable component of overall sampling effort; however, the number of trees climbed can be reduced by sub-sampling, without substantial loss of accuracy in the data (Caron & Fleming 1995). Ground-based
tation is often difficult, especially in luxuriant forests and when carrying sampling equipment. Canopy sys tems which are operated from the ground, for example pulley-operated mammal traps, can provide sampling resolution, but often demand a heavy time invest ment before sampling commences (McClearn et al.
in
pers. comm.). Distance ladder
limit the
rigging
ropes can also have an indirect effect on logistics. For example, sampling epiphytes
the position of rope (O.Missa, between
needed
effort
problems
nate
some
possible
cases,
it
constraints
is possible of access
to on
reduce sampling.
or
elimi Many
36 a combination
use
researchers
to extend
sampling
access-related
where
work
and acceptance
is important.
In such
cited
techniques
Alternatively,
to experimental
limitations
researchers
canopy
capability.
a recognition
be avoided,
access
of
cannot
of this by
cases,
as
text
in the
Canopy Research
exper
communications.
personal
We
are
also grateful for helpful comments by two anonymous reviewers. Funding for attendance (by MB) at the European Science Foundation conference on Tropical is acknowledged
with
thanks.
imental protocols need to be designed accordingly. The introduction of unfamiliar access techniques mean
may
that
cannot
researchers
easily
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Canopy
than one access method is possible, decisions need to be taken about the best combination of methods to achieve good sampling. Budget limitations may require the use of cost/benefit analyses to determine choice of access method (sensu Zandt 1994; see also 1973; Moffett & Lowman 1995; Barker 1997). In studies for which consistent sampling effort among trees is an issue, the effect of using different access
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mentation
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to
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Acknowledgements We
are grateful for the feedback provided by the nu
merous vey
canopy reported
contributed
researchers in this
paper.
additional
who
responded
In many
information,
cases,
to the
sur
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