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MOVEMENT AND DISTRIBUTION OF THREE SPECIES OF INQUILINE INSECTS IN BOREAL BOGLANDS: PROCESS AND PATTERN AT MULTIPLE SPATIAL
SCALES
by
MAFLGARET ANNABELLE KIWWCHUK -
B, Sc. (Hon) University of Guelph, 1995
Thesis submitted in partial füinllrnent of the requirements for
the Degree of Master of Science (Biology)
Acadia University S p ~ g Convocation 200 1
O by MARGARET ANNABELLE IKRAWCHUK, 2000
National Library I*l of Canada Bibliothèque nationale du Canada
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TabIe of Contents
........................... List of Tables .... ..................................................................................... vi
. . List of Figures .......................O...... ................. .................................................................. vil ...
Abstract ............ .......... .................................................................................................... vui
Acknowledgements .......................................................................................................... ix
General Introduction ............................ ......................................... 1
References ................................................................................................................ 12
Chapter 1 . Movement potential of Wyeomyio smitlzii (Diptera: Culicidae): pattern and process ....................... ... ........................................................................................ 14
Introduction .................... .... ......... ... .............................................................. 14
Methods ........................ .. ......................................................................................... 17
Results .................................................................... .................................................... 27
Discussion ............ .... ............................................................................................ 31
References ........................ ....... .................................................................................. 37
Chapter 2 . Movement potential of FIetc~zerm~iaJrefc~zeri (Diptera: Sarcophagidae): implications for the study of populations ............................ .... ..................................... 39
Introduction ............................. .................................... 39 ............................................. Methods ....................................................................................................................... 40
Results ....................... .... ..................................................................................... 42
Discussion .................................................................................................................... 43
References .................... ...... .................... ..................................................................... 45
Chapter 3 . The relative importance of habitat structure changes within a nested hierarchy of spatial scales for three species of însects .......................................... 46
........................ Introduction ... ............................................................................... 46
.................. Methods .. .............................................................................................. 49
Results ........................ ..... ........................................................................ 57
Discussion ................. ....................... ........................................................................... 64
................................................................................................................ References 71
Synopsis .................. ........................................................................... ..................... 74
Appendix 1 . Roosting behaviour by FIefcIzerimyioflefcheri (Diptera: Sarcop hagidae) ........................................................................ in Sarracenia purpurea (Sarraceniacea) 76
References ................................................................................................................ 79
List of Tables
Chapter One
Table 1-1 Variables and attributed values for the W. smithii diffusion model.. . . . . 25
Table 1-2 A summary of movement information calculated fiom W. srnithii
release-recapture experiment and diffusion modeling.. . .. . .. . .. . .. . .. .. . . 28
Table 1-3 Variance coniponents analysis of larval W. smithii abundance at
four spatial scaies.. . . . . .. . . . . . . . ..... . . . ... . . . .. . . . . . . . . . . . . . . . . . . . . 30
Chapter Two
Table 2-1 A summary of information fiom field collection and difision modelling
to estimate F. fletcheri and W- smithii movement potential. .. . .. . . . .. . . . . 43
Chapter Three
Table 3-1 A summary of larval sarnpling effort by spatial scale and sample period 50
Table 3-2 A summary of structural variables used in multi-scale sampling.. . . . . . . . 52
Table 3-3 A summary of glm output for W. smirhii .......................... .. ...... 59
Table 3-4 A summary of glrn output for M. knabi ...... ..... ... .. . . . .. . ... .. . .. .... . . 60
Table 3-5 A sumrnary of glrn output for F. fletcheri ............... .. .. . ..... .... ..... . . 61
Table 3-6 A surnmary of mixed-effects ( h e ) models for W. smirhii ....... . .. . ...... 62
Table 3-7 A s u m r n q of mixed-effects (lme) modeIs for M. knabi.. . . ... . . . . . .. . . . . 62
vii
List of Figures
Introduction
Figure 1-1 A map of Newfoundland indicating general study location.. .-.. ........ 4
Figure 1-2 A GIS representation of the no&-west area of the study sy stem.. ..... 5
.................................... Figure 1-3 The pitcher plant, Sarracenia purpzrrea. 7
Figure 1-4 Members of the Sarracenia. purpurea inquiline comrnunity .. - ......... 10
Chapter One
Figure 1-1 The proportion of Sarracenia pztrpurea plants per distance class
.......................... ....... occupied by Wyeomyia srnifhii lmae.. - 28
Chapter Three
............. .... Figure 3-1 A visual summary of study design and variables.. .-.. 53
Figure 3-2 Direction and scde of significant relationships behveen
PQeomyia smithii, iIïetriocnemz~s knabi, and Fletcherimyia fletcheri
................. . . . density and structural variables.. .. .... ... - . 63
viii
Abstract
This study explores the movement potentiai and distribution of three species of
inquiline insects, Wyeomyia smithii (Cdicidae) , Metriocnemus knabi (C hironomidae) and
Fletcherimyia fletcheri (Sarcophagidae). Movement potentiai was detennined using
empirical mark-recapture studies, mathematical diffusion models and variance
cornponents analysis, and the process of movernent was used to predict spatial scdes
relevant to individual and population dynarnics.
The larvae of ail three dipterans obligately develop within the leaves of the
pitcher plant, Sarracenia purpurea (Sarraceniaceae) providing naturally nested Ievels of
scale including leaves within plants within clusters (points) within bogs. With the
estimates of relevant spatial scales as a template, census of the three species was used to
assess the influence of habitat structure (amount and configuration of habitat) on insect
distribution within this discrete hierarchy of spatial scales. The S u e n c e of habitat
texture was estimated at a single scale. In general, species responded to amount of habitat
at relatively fuie (individual) spatial scales, and configuration of habitat at broader
(population) scales, though each responded at slightly different absolute scales. These
relationships corresponded to evolutionarily divergent attributes such as body size andlor
movement potential. This change in the importance of structure among species and scales
demonstrates that spatial scale is an imposant attribute to be considered in conservation
decisions.
Acknowledgements
Thank you to everyone! Especially Adele Mullie, Sonja Teichert, Michelle
McPherson, Julie McKnight, Sharon Midwinter, Dave Shutler, Derek Potter, Sheila
Potter, Joe Nocera, Trina Fitzgerald, Matéo Yorke, John Chardine, Soren Bondmp-
Nielsen, Marty Snyder, Andrea Kingsley. Special thanks to Matt Holder who put up with
me in close Gros Morne quarters for two whole summers, and never ceased to keep me
smiling and thinking. Also, Renée Cormier and Jen Miner for a brilliant sumrner in 1999
- run chickens nui! 1 am indebted to Brian Starzomski, Trish Turliuk and Kat Benedict
for keeping me grounded for parts of these two years. Phi1 Taylor provided so many
ideas, much encouragement and good Company - thank you'OO. Thanks M m , Dad and
Carolyn for your continuous curiosity and support.
Funding and support came ftom: Atlantic Co-operative Wildlife Ecology
Research Network (AC WERN), NSERC, Western New£oundland Mode1 Forest
(WNMF), Parks Canada (Gros Morne National Park), Environment Canada Science
Horizons Program, Newfoundland Department of Forestry Resources and Agrifoods
(Pasadena), Stephen Flemming and Scott Taylor at Gros Morne National Park, Corner
Brook Pulp and Paper Ltd, and Ransom (RAM) Myers (statistical advice).
Lastly, thanks to Leo Hynes for the wee cabin in the woods.
GeneraI Introduction
The spatial distribution of organisms is a result of many factors at multiple spatial
and temporal scales. For example, specific processes such as the movement or fecundity
of an individual typically affect broader-scale phenornena such as population persistence.
Thus, patterns of organism aggregation can be understood as emerging fiom the
collective behaviours of large ensembles of smaller scale uuits (Levin 1992). This
emergent pattern is Iimited by larger scale constraints such as competition or resource
structure (e.g., habitat or prey structure). The result is a continuous opposition between
biological potential and constraint that occurs dong a hierarchy of spatial and temporal
scales, reinforcing the view that there is no single natural scale at which ecological
phenornena should be studied (Levin 1992). One way to understand and ultimately to
predict the dynamics of natural systems, is to identie rnechanisms underlying patterns
(of distribution) and to determine what limits them and how they are constrained at a
variety of spatial scales.
Organisms typically prefer certain m e s of habitat, thus species react to variabihty
in environmental (habitat) structure. A conventional fundamental unit of structure is a
patch of habitat, whether studied at a broad (e-g., population) or fine (e-g., individual)
scale. In this context, environments can be imagined to consist of patches, defined as
follows: a discontinuity in environmental character states pertinent to the organism
(Wiens 1976); bounded, connected discontinuity in a homogeneous reference background
(Levin and Paine 1974); and, as any place in the environment where the abundance of
either resources or organisms is high or low relative to its surroundings (Roughgarden
1977). These definitions al1 incorporate the notion that there are areas that are 'more' and
'less' suitable to organisms. The habitat patch makes intuitive sense, but it is more of a
concept than an object (see Kotliar and Wiens 1990; Bowers and Matter 1997), since
absolute boundaries of a patch are often difficuIt to delineate.
One method to approxirnate a patch of habitat relevant to an individual or group
of organisms is to understand the processes which support patterns of organism
distribution in the environment (also described as an ecological neighbourhood in
Addicott et al. 1987), and thus to determine the "grain" (the srnailest scale at which an
organism responds to patch structure) and "extent" (the largest scale of heterogeneity to
which an organism responds) relevant to the organism (Kotliar and Wiens 1990). In
doing so, habitat patches are biologically meaningfid to the study organism can be
defrned. As a result, estimates of habitat, or landscape structure can be scaled
appropriately to match definitions of individual or population dynamics.
Ecological studies ranging from spatially explicit metapopulation models of
organism distribution to a simple assessrnent of habitat use by organisms, evaluate the
relationship between process and/or pattern of organisms and their environment. The
structure of the environment c m be represented theoretically by an infinity of measures,
but landscape ecologists typically describe habitat (patch) structure using a parsimonious
trio including: composition (arnount), configuration and connectivity (Dunning et ai.
1992; Taylor et al. 1993). This mems that the composition (or arnount of each patch
type) dong with its position in space, and the nature of the space between patch types,
respectively, is hcluded in the description of the landscape. In practice, a suite of
measurable features can be estimated to represent these three concepts (see Forman and
Godron 1986; Wiens et al. 1993).
In this study 1 attempt to describe and understand the observed spatial pattern of
distribution of three species of insects, Wyeomyia smithii, Metriocnemus knabi and
Flercherimyiafletcheri. I use two approaches. First, by studying the process of individual
movement and estimating movement potential (for two of the three species; Chapters One
and Two), 1 predict spatial scaies relevant to individual and population dynamics. ln
addition, 1 propose links between movement potential, behaviour, and spatial pattern.
Second, by relating the distribution of the study organisms to habitat structure at multiple
spatial scales, I explore the influence (or constraint) of amount, configuration, and texture
of habitat on both individuals, and aggregations of the study species (Chapter Three). 1
compare response to structure at different spatial scales both intra- and inter-specifically,
incorporating movement potential as a process generating these relationships.
Study system
This work was done within the watersheds of the Main and Humber Rivers in
western Newfoundland. (UTM: 5514000N 478000E Zone 21U), an area of old-growth
(pers. cornrn. John McCarthy) boreai forest east of Gros Morne National Park (GMNP)
considered part of the Gros Morne Greater Ecosystem (GMGE) mg. 1-1). Research
activity is accelerating Iargely due to proposed forestry activity in the area. The long-term
impact of forestry on the region is unknown, but it has the potential to influence the
persistence of natural populations of plants and animals, and the ecological integrity of
G W .
Figure 1-1. A map of Newfoundland, Canada indicating the general location of the study
system. Gros Morne National Park is shaded in black on the western coast of the island,
the study site is delineated in white.
Figure 1-2. A GIS representation of the north-western area of the study Iandscape. This
naturally heterogeneous forest is cornposed of discrete bogs within a "rnarrix" of boseal
forest. Bogs are represented by yellow, water by blue, 'harvestable' forest by green, and
softwood scmb by beige. Map courtesy of Corner Brook Pulp and Paper Ltd.
This boreal landscape is a naturally heterogeneous area composed of discrete
patches of bog, mature coniferous forest (Balsam fir, Abies balsamea, and Black spruce,
Picea mariana) and softwood scrub (A. bdsamea and P. mariana) with nurnerous ponds
and rivers throughout (Fig. 1-2). The bogs are primady composed of Sphagnurn spp.
rnosses and contain extensive areas of shrubs and numerous flowering plants.
Bogs provide habitat for the pitcher plant, Sarracenia purpurea L.
(Sarraceniaceae; Fig. 1-3), a camivorous, perennial plant specializing in nitrogen-poor
environments. A large body of knowledge exists pertauiing to S. pzirpzirea and the
comrnunities which exist in its fluid-filled leaves. Sarracenia purpureu are abundant in
most boreal bogs but Vary greatly in plant density, size and condition. The plants can be
clustered together or isolated by tens of meters; leaf size and the nurnber of leaves per
plant are also variable. The plant flowers in July and August and not every plant produces
a flower in a given year.
Three species of fly, a mosquito, Wyeomyia smithii Coq. (Culicidae), a midge,
Metriocnemus krzabi Coq. (Chironomidae) and a sarcophagid, Fletcherimyia fletchéri
Aldrich (Sarcophagidae) have an obligate relationship with S. purpurea (Figure 1-4). The
eggs a d o r larvae of these three species inhabit the fluid-filled leaves of the plant during
their development. A mutualistic relationship exists between the plant and these
inhabitants whereby the larvae accelerate breakdown of prey and the rate of amrnonia
production in the leaves of S. purpurea wkle the leaves infuse oxygen into the water they
contain (Bradshaw and Creelman 1994). Sarracenia pupurea does not release digestive
enzymes into the fluid within the Ieaf. Characteristics of S. purpzrrea leaves that have
been linked to inquiline abundance include leaf age, actual and potential volume of fluid,
and the amount of organic matter. However, these characteristics exphin less than half
the observed variation in larval abundance (Nastase et ai. 1995) suggesting either
excessive random variation or that additional influentid factors exist.
Figure 1-3. The pitcher plant, S. purpzrrea. The larvae of W. smithii, M. knabi and F.
Jetcheri obligately develop within the leaves of the plant (a). Adult F. ji'etcheri roost and
mate within the flowerheads of the plant (b). Line drawing taken from Peterson and
McKenny (1968).
Wyeomyia smithii is a small culicid mosquito roughly 3 mm in length. Females
are autogenous in the norîh (do not require a blood meal for ovarioIar development
(Smith and Brust 1971 ; 07Meara et al. 198 1)) and deposit small ciutches of eggs into the
leaves of the pitcher plant in rnid-summer (Mogi and Mokry 1980; 07Meara et al. 1981).
Within the leaf fluid, the eggs hatch and develop to third instar larvae before entering
diapause and over-wintering (Smith and Brust 1971). Over-wintering mortality is
increased when temperatures of less than -5°C are experienced for more than four
months, thus snow cover is necessary for over-wintering survival (Smith and Brust 1 97 1 ).
The species is univolthe in its northern range, and individuals emerge synchronous~y in
Newfoundland in late June, early July (Heard 1994a, b; Miner 1999; pers. obs.). Thus, the
population distribution resulting fiom movement of addt females emerging in mid-
summer c m be measured by looking at the distribution of larvae in late summer.
The sarcophagid fly, Ffletcheri is a larger fly (7.5 mm in length) similar in stature
to the bouse fly, Musca domestica. In previous studies the fly was referred to as
Blaesoxipha (F.)fTetcheri. We refer to it by its current scientific names. The larval stage
of F. fletcheri has been studied more thoroughly than the adult. Since larvae are intra-
specifically aggressive, occupancy in leaves does not usually exceed one lama (Forsyth
and Robertson 1975). Adult female F. fletcheri larviposit directly into the leaves of S.
pzïrpzrrea in rnid- to Iate summer. Larvae develop in the pitcher's fluid until light and
temperature cues initiate pupation. Larvae move out of the leaf in fall, and pupate, over-
wintering in the Sphagnum spp. rnoss fiom which they emerge the following sumrner
(Forsyth and Robertson 1975; Hardwick and Giberson 1996). Adults roost in S. purpurea
flowers through the night (Krawchuk and Taylor 1999) where they have also been
observed rnating (for up to three hours (pers. obs.)). The adults are easiIy sexed externally
by observing the genitalia and shape of the abdomen, females being much broader than
males (pers. obs.).
The niidge, M knabi, is a s rnd chironomid. The Ianrae have been observed in S.
purpurea leaves throughout the surnmer (Paterson and Cameron 1982, Hardwick and
Giberson 1996; Rango 1999; pers. obs.), but peaks in abundance in Newfoundland occur
in Iune and again in August (Heard 1 994a,b; Miner 1 999). Paterson and Carneron (1 982)
suggested that A4 knabi dynarnics operate within an overlapping three-year cycle
whereby females fiom a May emergence oviposit into leaves and produce a generation
which emerges in August. The progeny of the August emergence develop and do not
emerge until the following July, this generation emerges the following May. Four instars
develop withui the leaves and prepupal instars crawl up the walls of the pitcher and
pupate in a gelatinous mass (Paterson and Carneron 1982; pers. obs.) above the fluid-line
fkom which they emerge.
The comrnunity interaction between these three species has been studied
extensively and has been described as a processing chain commensalism (Heard 19946).
Midge larvae feed by chewing on solid material, while mosquito lanlae filter-feed on
particles derived fiom the decaying matter and directly on bacteria. Sarcophagid larvae
are buoyant and feed upon newly captured insects floating upon the surface (Fish and
Hall 1978). niere does not appear to be an obligate relationship between the species, nor
a competitive one. While l a n d information is abundant fkom studies of inquiline
comrnunities, little is known about adult behaviou or life history.
Figure 1-4. Community living: a schematic representation of members of the Sarracenia
purpurea inquiline community including A) Wyeomyia srnithii (adult); B ) W. smithii
(Iarva); C ) ikfetriocnemus knabi (adult); D) M. knabi (larva); E ) Fletcherimyia fletcheri
(adult); F) F. j7etcheri (lama). Diagrams represent general morphology of the family, not
the species. Line drawing were reproduced fiom McAlpine et al. (1981).
Miner (1999) provided invaluable prelirninary work on the system with a study of
relationships between both insect abundance and plant morphology, and two components
of landscape structure (bog size and closure, the height of trees surrounding the bog) in
coastal Newfoundland. Miner's (1999) study demonstrates that bog size and the degree of
protection fkom winds (measured as closure) signincantly influences plant morphology
and midge, mosquito and sarcophagid abundance. Further, Miner (1999) proposed
relevant levels of spatial scale for the study of W- smithii and M h a b i populations based
on variation in abundance within nested spatial scales.
In this study, 1 measure movement potential of W. smithii and F. fletcheri
explicitly using release, or mark recapture (respectively) experiments to confirm and
fUrther explore behavioural and spatial patterns inferred from Miner's (1999) study.
Further, 1 use three conventional measures of habitat structure: the arnount, ~onfl~pration
and connectivity (vegetation texture) of habitat to determine hou; members of the S.
purpzrren inquiline cornmunity respond to structure at multiple spatial scales.
References
Addicott, J.F., Aho, J.M., Antolin, M.F., Padilla, D.K., Richardson, J.S. and Soluk, D.A. 1987. Ecological neighborhoods: scaling environmental patterns. Oikos 49340- 346.
Bowers, M.A. and Matter, S.F. 1997. Landscape ecology o f mammals: relationships between density and patch size. J. Mamrnal. 78:999-lO 13.
Sradshaw, W.E. and Creelman, R.A.. 1984. Mutualism between the camivorous purple pitcher plant and its inhabitants. Am. Midl. Nat. 112:294-301.
Dunning, J.B., Danielson, J.B. and Pdliam, H.R. 1992. Ecological processes that affect populations in complex landscapes. Oikos 65: 169- 1 75.
Fish, D. and Hall, D.W. 1978. Succession and stratification of aquatic insects inhabiting the leaves of the insectivorous pitcher plant, Sarracenia purpurea. Am. Midl. Nat. 99:172-183.
Forman, R.T.T. and Godron, M. 1986. Landscape Ecology. Wiley, New York. Forsyth, A.B. and Robertson, R.J. 1975. K reproductive strategy and larval behavior of
the pitcher plant sarcophagid fly, Blaesoxiphafletcheri. Can. J. Zool. 53 : 174- 1 79. Hardwick, M.L. and Giberson, D.J. 1996. Aquatic insect populations in transplanted and
natural populations of the purple pitcher plant, Sarracenia purpzrrea, on Prince Edward Island, Canada. Can. J. 2001.74: 1956- 1963.
Heard, S .B. 1994a. Pitcher-plant midges and rnosquitoes: a processing chah cornmensalism. Ecology, 75: 1 647- 1660.
Heard, S.B. 1994b. Imperfect oviposition decisions by the pitcher plant mosquito (Wyeomyia smithii). Evol. Ecol. 8:493-502.
Kotliar, N.B. and Wiens, J.A. 1990. Multiple scales of patchiness and patch structure: a hierarchical framework for the study of heterogeneity. Oikos. 59:253-260.
Krawchuk, M.A. and Taylor, P.D. 1999. Roosting behaviour by Fletcherimyiafletcheri (Diptera: Sarcophagidae) in Sarracenia purpurea (Sarraceniacea). Can. Ent. 13 1:829-830.
Levin, S.A. 1992. The problem of pattern and scale in ecology. Ecology 73 : 1943-1967. Levin, S.A. and Paine, R.T. 1974. Disturbance, patch formation and community structure.
Proc. Nat. Acad. Sci. U.S.A. 7 1 :2744-2747. McAlpine, J.F., Peterson, B.V., Teskey, H.J., Vockeroth, J.R. and Wood, D.M. 198 1.
Manual of Nearctic Diptera. Canadian Governrnent Publishing Centre, Hull Quebec.
Miner, J.A. 1999. The influence of landscape structure o n the distribution and dynarnics of insect comrnunities inhabiting the leaves of the purple pitcher plant (Sarraceniapurpurea). Hons. Thesis. Acadia University, Wolfville, Nova Scotia.
Mogi, M. and Mokry, J. 1980. Distribution of Wyeomyia srnithii (Diptera, Culicidae) eggs in pitcher plants in Newfoundland, Canada. Tropic. Med. 22: 1-1 2.
Nastase, A.J., de la Rosa, C. and Newell, S.J. 1995. Abundance of pitcher-plant mosquitoes, Wyeomyia smithii (Coq.) (Diptera: Culicidae) and midges, Metriocnemus knabi Coq. (Diptera: Chironomidae), in relation to pitcher characteristics of Sarracenia purpurea L. Am. Midl. Nat. 13 3 :44-5 1.
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Chapter 1. Movement potential of Wyeornyiu smifltii (Diptera: Culicidae): pattern and process.
Introduction
An assessment of the movement potentid of organisms (either of individuals or
their gametes) is an important component of ecological data interpretation and prediction
(Levin 1992; Turchin 1998). Studies of processes such as movement, fecundity or habitat
selection provide valuable information on natural history and evolutionary patterns.
Collectively, incorporation of the mechanisms contributing to spatial pattern into studies
c m help us mode1 population aggregations more realisticaüy, make wiser management
decisions and design future research at appropriate spatial and temporal scales. For
example, Griinbaum (1992) used individual-based modeling of krill populations to
dernonstrate that the collective behaviour of individuds gives rise to the formation of
aggregations consistent with field observations. By exploring variable mechanisms that
generate and maintain patterns we rnove fiom a deductive observation of pattern, towards
an inductive appreciation of the underlying complexity of the system. This mechanîstic
understanding also clarifies the relative importance of processes driving patterns at
multiple spatial and temporal scales, an extremely important topic in ecology and for our
comprehension of ecosystems (Kotliar and Wiens 1990). The overall importance of this
concept is M e r highlighted by curent work in a vax-iety of disciplines inciuding
biology, physics and economics, that similarly focus on the links between process and
pattern (Levin 1 992).
Movement is a cntical process aEecting populations by increasing genetic
variability, rescuing popdations fkom extinction, allowing colonization of new habitat
and altering species interactions (Turchin 1998). Mathematical quantification of
movement enables us to simpl% the process, and to transform it into a powerful
predictive tool in population ecology. The use of diffusion models to explain movement
pathways of organisms is one of the most successfül applications of mathematics to
ecological phenomena (Levin 1992). For example, Kareiva (1983) found that the Local
dispersal of eight of twelve species of herbivorous insects in simple environments could
be adequately described by simple difision. Spatial heterogeneity tends to increase with
higher levels of scale as a result of structural patchiness in habitat. In the context of a
heterogeneous landscape, movement may be remarkably different within and between
patches of suitable habitat, reflecting the influence of habitat structure. Flexibility in the
diffusion template allows pertinent addition of mathematicai complexïty to accomodate
heterogeneity into equations at a variety of spatial scales.
Frequently, populations of organisms using a heterogeneous landscape can be
described as a metapopulation system. Metapopulation theory describes the broad-scale
pattern of organisrns within population-level habitat patches whose independent
dynamics are driven by colonization and extinction events (Levins 1970; Edwards et al.
1994; Hanski and Gilpin 1997; Thomas and Kunin 2999). Though a continuum of
metapopulation scenarios exist (Harrison 1994), each describing varying degrees of each
population's independence £tom the other, an assurnption common to al1 scenarios is that
movement arnong groups ensures the persistence of the overall metapopulation. In the
context of rnerapopulations, the measurement of an organism's rnovement potential
allows us to consider whether interaction among (spatially distributed) habitat patches is
theoretically possible. In hm, this indicates which spatiai scales are reievant to studying
population or metapopdation persistence. Thus by understanding the movement process,
we more fully understand the spatial scde of within and between patch dynamics.
Further, this information can be used to predict how organisms might respond to the
structure of their environment.
The hierarchically "patchy" resource structure of the pitcher plant mosquito,
srnithii, in the bored forest of western Newfoundland suggests that population dynamics
could be described in a metapopulation framework. This "patchiness" can be visualized
as discrete leaves on plants, plants in a cluster, multiple clusters of plants distnbuted in a
bog, with discrete bogs embedded in a "matrix" of coniferous forest. However, the
appropriate spatial scale at which to study metapopulation-type dynamics depends, in
part, on the movement potentid of W. smithii. Similarly, the relationship between these
nested levels of habitat structure and the distribution pattern of W- srnithii may be
integrally related to the ability of the mosquito to move between and within patches of
resources.
In light of these ideas, there were three objectives to this study: one, to mode1
empirically derived movement data using diffision-theory equations to determine if
simple mathematical models could adequately describe the movement patterns of W-
srnithii within patches of bog habitat; the moments fiom these equations codd be used in
future predictive modeling of the system; two, to suggest the appropriate scale for
studying (meta) population dynamics of W. srnithii using a suite of indicators including
difision equations and distribution patterns fiom large scale census data; three, to
address a gap in natural history information pertaining to the movement potential of W.
smithii. An extensive base of literature provides information concerning the three-
member uisect community inhabithg S. purpureu, including a vast amount of
information about population and community dynamics within the leaf of the plant itself.
However, to our knowledge there is no empirical irformation available on rnovement
ability of the insects.
1 addressed these objectives using two methods. 1 used a release-recapture
experiment to measure movement potential of W. smithii explicitly. These data were used
in the diffusion rnodel and as traditional statistical descfptors of movement distance. 1
used a large scale census of W- smithii distribution to infer movement using variance
components analysis.
Methods
Release-recapture field procedure
The movement potential of W. smithii was estimated using a release-recapture
experirnent designed to measure the distribution of W. smithii larvae resulting fiom
successfUl emergence, mating, movement and oviposition by adult femaies which were
deposited as larvae at the release site. This design required a bog containing no W. smithii
larvae pnor to the study period, either natwally or through the removal of existing larvae
pnor to the experiment.
An experirnental bog was chosen after initiai sampling of the inquiline
cornrnunity in 150 pitcher plants (3 leaves per plant, n=450) indicated an absence of W.
smithii larvae in the area - ideal conditions for the movement experiment. Larval W.
smithii were detected in al1 of 40 additional sample bogs in the area (see large scale
sampling that follows) fiom a sarnple effort of between six and 24 plants per bog,
suggesting that 150 plants was an adequate effort. A sarnpling grid was constnrcted
consisting of a geo-referenced release line, and three geo-referenced transects each with
sampling points extending 200 rn in both directions perpendicular fkom the release Iine
(six transects). The grid contained 78 sampling points (234 plants) in total which were
positioned at intervals between 10 and 20 m apart along the six transects. Each sample
point consisted of the three pitcher plants, the nearest three viable plants to a flagged
point (plants were always within five rneters of the flagged point). These points were
used to sample the redistribuîion of larvae.
On 6 Jdy 1999, 840 W. smithii larvae (7 20 pupae plus 130 fourth instar larvae
were coliected fiom nearby bogs within 10 km) were deposited in 84 pitcher plant Ieaves
distributed randornly along the full length of the release line. Ten individuals were placed
in each leaf to approximate densities reported in previous experimental studies of W.
smithii (Heard 1994). To determine an appropriate re-sampling date, the progression of
development and emergence of released larvae was monitored in randornly chosen
release leaves during £ive visits to the bog between the release date (6 July 1999) and the
recapture-sampling date. Three weeks after pupation of larvae was observed, recapture-
sampling was initiated at the experimental bog. RegionaI phenology of I;TI srnithii was
also monitored at a permanent sampling bog one kilometer from this experimental bog.
First and second instar larvae were detected consistently at the permanent sarnpling bog
concurrent to the re-sampling of the experimental bog, corroborating the validity of
timing for the resample.
Re-sampling occurred on 26 August 1999. Three recapture-sample leaves were
chosen from each sample plant (n=702 Ieaves) based on their age and condition. Each
leaf was the current years' cohort, held water, and had a distal opening large enough for
the entrance by adult W- smithii. Each leaf was removed fiom the plant and the contents
were poured into a sorting tray. The leaf was opened and al1 plant and animal material
was flushed to the tray with water. The abundance of larvae according to leaf, plant and
point was recorded and associated with the measured distance fkom the release line. Two
distance-distributions of larvae were recorded. The first distribution described the
perpendicular distance fiom the release line to the point of capture. The second
distribution described the maximum distance from m y point on the release line to the
capture location. The perpe~dicular distance distribution assumes that individuals move
directly out fiom the release line, a minimum; while the maximum move distance likely
over-estirnates movements closest to the release line. These two methods will provide an
approximate range in movement estimates, since direct observation of movement was not
possible.
In addition to the sarnpling scherne detailed above, two other methods of
recapturing W. srnirhii were attempted, but proved unsuccessfid. First, the interior
circdexence of leaves were coated with Tanglefoot (Bioquip, California) in an attempt
to trap adult female W. smithii while ovipositing at pitcher plants. Circular coverage of
the leaf was one centimetre (height), including and just below the level of the ventral lip
of the leaf. Only one W- srnithii specimen was captured using this technique, however,
many other specimens of Coleoptera, Hymenoptera, Diptera and Arachnida were
recovered in good condition. The second method involved covering the top surface of
cork discs (two mm high) with Tanglefoot and placing the discs to float at the surface of
fluid in purpurea leaves. Similarly, many insects, but no W. smithii, were coilected in
good condition
The diffusion mode1
The diffusion equation used to explore the K mithii recaphne-sampling data was
based on a simple model for time-integrated data discussed explicitly in Turchin and
Thoeny (1993) and Turchin (1998). The model dehes C, the total catch in a trap (as time
+ 4 as,
where D is the diffusion rate, 6 is the disappearance rate of animais (e.g., a result of
death), a is the effective sampling rate of traps, No is the total number of organisrns
released, and x is the distance fiom the release point.
Drift
For bi-directional rnovement &a f?om the release line to be combined within the
uni-directional model the assumption that no drift existed Ui the data needed to be tested.
If no drift existed, the position of recapture-sampled larvae was equally likely to occur in
either direction fi-oom the release line. 'Population' drift would cause a shift in the average
displacement from the ongin, which in tum would be refiected in the spatial distribution
of recaptures (Turchin and Tizoeny 1 993). Displacement of recapture-samples X, was
calculated as,
where C(x) is the abundance of larvae at a sampie point, x is the x coordinate of the plant
location (modified for direction as +l- displacement), and n is the number of points
sampled. We tested the hypothesis of no drift (X not different ftom zero) using a t test
(MathSofi Inc. 1999).
Mode1 fitting
Raw data fiom both distributions (perpendicular and maximum distance) were
Poisson distributed once they were pooled to be uni-directional. Due to the small number
of larvae obtained fiom the recapture-sampling, data were interpreted at the scale of the
plant and manipulated to provide a response variable representing the proportion of plants
occupied within each distance class. Based on observation of weak female £light
(Bradshaw 1983; lstock and Weisburg 1987; pers. obs.) and the abundance of plants in
the study area, each larval incidence at a plant was considered to represent an
independent fernale. Previous studies suggest that an adult female deposits one to three
eggs at each visit to a leaf (Mogi and Mokry, 1980; Heard 1994).
Since a 'trap' in the original mode1 infers that animals stop moving after
encounter, the meaning of a was rnodSed to represent the deposition of eggs by female
W. smithii. This modincation is inspired f b m work by Okubo (1980)' who madeled the
distribution of uisect eggs in space as a result of adult movement, thus accounting for
continued movement of a female after laying eggs o n h the host plant. Similar examples
of equation modifications can be faund in Williams (1961) and Broadbent and Kendall
(1953); Williams (1961) uses a two dimensionai Bessel function, as opposed to this one
dimensional form, but the logic is identical. As a result, a now represents the rate of
larval deposition (W smirhii oviposlt, but since larvae were counted, hatch rate of eggs to
larvae waç included in the calculation of a).
A further modification to the original equation was made to account for
manipulation of the response variable C(x) fiom an abundance per plant leaf at distance x
to a proportion of plants occupied within distance class (6). The working equation is,
where 4 represents the number of plants sampled in distance class d. The value of a was
determined using literature-derived infurmation (Table 1 - 1). The total number of larvae
released was known, and d was determined for each plant sampled using real-time
corrected GPS (Trimble Surveyor TDCZ, Trimble Inc. California); distance classes were
categorized in five meter intervals. The models were & using an iterative nonlinear least
squares model (nls) in S-PLUS 2000 (Venables and Ripley 1996) fiom which estimates
of the parameters 6 and D were cdculated.
The rnean and variance of move distances were predicted using the diaision
paraneters calculated in E q d o n 3. The estimate of mean move distance (for
perpendicular and maximum distance distrriutims) for W- mithii (ab., time integrated)
w=,
using the derived diffùsion rate, D. This equation predicts a two dimensional move
distance based on the dimensions of a circle, however it is still a valid calculation since D
and 6 were appropriateIy derived fiom the data, though in one dimensional space. The
variance in move distance for W: smithii was estïmated as,
In addition to fitting the data to the df i s i on model, Equation 3, they were also fit
to a generic exponential model (sensu Theony and Turchin 1993),
where C(d) is the proportion of plants occupied by Iarvae within a distance class d. The
relative fit of the two models (Equations 3 and 6) was compared quantitatively using
residual deviance.
The data were compiled fiom the release-recapture experiment using traditional
statistical descriptors to observe general patterns and lUnits in the data including the
minimum, maximum, mean, and median move distance. These values were used to v e w
and assess the diffiision rates predicted by the difhsion models.
Table 1-1. Variables and attributed values used to estimate a (rate of larval deposition)
in the W- smithii difision mode1 (Equation 3).
Variable Source Eclosion success 0.45 Kleckner and Bradshaw 199 1 Emergence success 1 .O0 Price 1958; Istock et al. 1975 Sex ratio (ma1e:fernale) 0.50 Istock et al. 1975 Mating success 0.50 estimated Mean eggs produced per fernale $ 62.00 pers. obs. (fiorn dissections) Correction factor Y 0.33 Mogi and Mokry 1980; Heard 1994 Hatch rate of eggs 0.80 Price 1958; Istock et al. 1975;
EUeckner and Bradshaw 199 1 Product of values (a) 1.84 $ Dissection, and ovariolar counts of eight fernale W. smithii were used to estirnate female fecundiv. Y Since Our response is the proportion of plants occupied per distance class (regardless of the number of larvae per plant), this value scales-dom the egg nurnber produced per female. The literature estirnates that a female commonly deposits between one and three eggs per leaf-visit.
Large scale sampling and variance components analysis
The distribution of variation from census of Iarval counts was used to estimate
movement potential of K srniihii. Vûriance components analysis (VCA) is used to
determine the distribution of variance between a variety of (random) factors in a study
design (Searle et al. 1992). In a VCA, peaks of unusually high variance are suggested to
indicate scales at which between-group differences are especiaily large, inferring the
scale of movement, natural aggregation or patchiness (Greig-Smith 1952, 1979). Here,
the f i s t purpose of the VCA tvas to determine the dominant spatial scale(s) of variation
in the W. smithii census data The second purpose was to determine if the magnitude of
scale of W. smithii movement potential inferred statistically through VCA corroborated
with movement parameters derived fiom the experimentai data and diffusion model.
Data for the VCA were collected fiom two multi-scale censuses of S. purpurea
larval cotumunities that took place concurrently to the experimental movement study
outlined above (Sample One: 5 June - 27 June 1999; Sample Two: 17 August - 25 August
1999). Briefly, the insect fauna were sarnpIed fiom the leaves of S. purpurea in 40 bogs
within 20 km2 region. Within each bog, between two and eight sampling points were
chosen dependant on the size of the bog. A point consisted of three viable purpurea
plants (nearest neighbours) and complete faunal samples were taken fiom the three leaves
of each plant using the same method as the recapture-sampling in the movement
experiment described above. These sarnples have spatial attributes of the following
factors: a leafwithin a plant, a plant within a point, a point within a bog, a bog within a
landscape. Local habitat characteristics were also measured with each leaf sample and
included: the amount of detritus in each leaf, the number of midge larvae (M. h a b i ) ,
number of sarcophagid larvae (F. ji'e'etcheri), and the actual and potential volume of fluid
within each Ieaf.
Generalized linear models (glms) in S-PLUS 2000 (MathSoft Inc. 1999) with a
Quasi-likelihood family wcre used to statisticaily "strip-away" variation of the leaf-level
habitat variables (e.g., actual fluid volume, community structure, amount of detritus) on
the abundance of W. smithii larvae in each leaf (see Chapter R e e for more details).
Sirice larval counts are an index of adult density, the residuals fiom the glrn were used as
a relative abundance (density-type) response measure in the variance cornponents
analysis (varcomp in SPLUS 2000).
Results Table 1-2 outlines the general movement parameters of the W. smithii mark-
recapture data. The raw abundance data indicated no drift in the distribution of larvae
fiom the release line using a one-sample t test (t=1.12, df=77, p=0.26) with a nul1
hypothesis that the true mean of the spatial distribution of larvae was equal to zero.
The nonlinear models (ds) of the distance-proportion data using the difision
equation (Equation 3) resulted in a reasonable fit to the field data @oth perpendicular and
maximum distance), suggesting that the estimates of values for a were adequate (Fig. 1-
1). The residual standard error after curve fitting was 0.049 (de24) for the perpendicular
distance distribution, and 0.06 1 (de241 for the maximum distance distribution. The
parameters (e-g., mean distance) calculated fiom the diffusion values matched field-
values quite closely (Table 1-2) using both distance distributions. The exponential model,
Equation 6, was fit to the perpendicular distance data using the same, nonlinear (nls)
routine for ease in comparing the fit of the two models (difision and exponential).
Again, a reasonable fit resulted Fig. 1-1). The parameter a (kl SE) was calculated as
0.72 k 0.14 ( ~ 5 . 0 0 ) ~ and b as 0.10 I 0.022 (t4- .70). The residual stmdard error after
curve fitting was 0.054 (dfX4).
Table 1-2. A summary of movement infom~.tion calculated fiom W. srnithii release-
recapture experiment and difision modeling.
Variable Value Source
Larvae introduced Leaves sampIed Larvae 'recaptured' Median distance of 'recaptures' Mean distance of 'recaptures' (41 SE) Maximum distance moved Disappearance rate (S+1 SE) Igeneration Diffusion rate @f 1 SE) / generation Mean distance moved Variance in distance moved
Recapture rate Estirnated disappearance rate
perpendicuiar 840 702 (234 plants) 37 2 m 1 0 t 3 r n 83 rn 0.0035I 0.00 1 1 0.17f 0.016 10.95 rn 74.56 rn
maximum 840 from release experiment 702 from release experïment 37 from release experiment 40 m from reIease experirnent 45k4 rn from reIease experiment 106 rn from reIease experïment 0.020k0.026 predicted by Eqn. 3 1.53+1.17 predicted by Eqn. 3 13.73 rn predicted by Eqn. 4 1 17.4 m predicted by Eqn. 5
3.7 % 3.7 % A/(B * C) 0.38 0.38 from release experiment
(1-((AE)*F)/B*c) A Number of larvae recaptured B Nurnber of larvae introduced C Rate of egg deposition and IarvaI survivorship per larva introduced (Table 1-1). E Nurnber of plants sampled (234) F Estimated r&nber of plants in the experimental bog frorn density transects.
3 4
Distance from release tine (In(rn))
B) Distance from release line (In(rn))
Figure 1-1. The proportion of S. purpurea plants per distance class occupied by
srnithii larvae (0 ) from field data collected in the release-recapture experiment. Data are
fiom A) the perpenciicular distance distribution, B) the maximum distance distribution.
Fitted values fiom the diffusion model (+; Equation 3) and the exponential model (C l ;
Equation 6) are also indicated.
Variance Components Analysis
The glms describing data collected in the two large-scale sampling sessions (June
and August 1999) suggested significant leaf-level effects of potential fluid volume, actual
fluid volume, detritus, and the interaction of potential and actud fluid volume on W.
smithii larval abundance (Table 3-3). Variance components analysis of the glm residuals
incorporating the four spatial factors hierarchically @og, point, plant, leaf) indicated an
unequal distribution of variance between these random spatial factors (Table 1-3).
Table 1-3. The percent variance in larval W. smithii relative abundance resoIved by
variance components analysis at four spatial scales: bog, point, plant, and leaf fiom a
large-scale census of their distribution. The distribution of variance was calculated for W.
smithii in two sessions (Sample 1 : 5 June to 27 June 1999; Sample 2: 17 August to 25
August 1999).
Census Bog Point Plant Leaf Sample 1 2.9% 20.5% 12.8% 63.7% Sample 2 3 -7% 12.9% 8.1 % 75.3%
Discussion
The goal of this study was to determine the movement potentiai of W- smithii
using both experirnental (release-recapture) and inferential (VCA) methods, and to
determine whether W. srnithii movement could be described by simple diffusion
equations. The imrnediate application of the movement data collected here was to
approxhate the appropriate spatial scale to study individual, population and/or
metapopdation dynamics of W. srnithii in the boreal forest region of western
Newfoundland. Parameters of move distance estimated for W. smithii by the diffusion
mode1 and basic statisticai descriptors of the field data suggest that females fiequently
move within and between patches of S. purpurea in a bog (up to 106 m), but that longer
movements through boreal forest between bogs would be infi-equent. The variance
components analysis M e r supports this scale of movement.
Diffusion equations can be extremely valuable tools in simulation experiments to
explore population and community patterns. However, they must be biologically robust if
they are to provide meaaingful output or predictive power. The data fiom the
perpendicular and maximum move distances were used to identiQ a range of movement
potential for W. srnithii. They provide an estirnate of relevant movement scale for W.
smithii of between two to 100 metres in a generation. The observed distribution of the
data fiom the perpendicular and maximum distance distributions resulted in a wide
spread of mean and median move distances, yet both distributions predicted similar mean
movement distance fiom the diffusion equations. Likely, this is due to the similar relative
distribution of observations. The fitted values fiom the equations approximated observed
within-bog movement rates fiom release-recapture data, suggesting a biological relevance
of the parameter, D (diffusion rate). This is further supported by the overlap in the range
of values for D, as indicated by the standard errors of the estirnates estimated fiom both
the perpendicular and maximum distance distributions. Though the overall fit of the
models is adequate, the parameters 6 (disappearance rate) calculated by the equation
differed fkom the observed field rate estimated fiom the release experiment by two orders
of magnitude, suggesting that M e r work be done in this area if the rate is to be used
predictively .
The fitted-values produced by the difision model using the perpendicular data
were very sirnilar to the values of the generic exponential model. Both equations appear
to represent the pattern of the field data equally well. However, while the exponential
model is more straightfonvard to produce, the biologically meaningful parameters
(diffusion and disappearance rate) derived fkom the difision model make it a
functionally superior equation.
The most variation in larval abundance existed between Ieaves, even after leaf-
level covariates representing differential habitat selection by individual females based on
leaf quality and cornrnunity structure were removed. This suggests that individual
females oviposit at a leaf, then move to a neighbouring plant, rather than ovipositing
consecutively in leaves within the sarne plant. Further, it suggests that leaf resources are
not used to capacity, and that larval numbers are somehow constrained either by an
unrneasured factor or at another scale. Less variation in larval numbers between plants at
a point than at leaves or at points within a bog m e r implies that females fkequently
move between these plants to oviposit, while the increased variation between points in a
bog suggests that the points are more independent (i.e., movement by female W. smithii
between points is not as Eequent). Though variation between bogs appears !ow in the
VCA, suggesting fiequent between bog movemrnt, bog aggregations likely operate
independently. Stronger point and le&-level aggregation outweighs variation between
bogs. Further evidence for independent dynamics between bogs is provided by genetic
analysis of W- smithii in the northem U-S,, which suggests fiee recombination at the level
of a whole bog (Istock and Weisburg 1987) and not beyond.
In concert, the data indicate that population structure of W. smithii exists at the
spatial scale of the bog, and that multiple, 'patchy' populations likely exist within bogs.
Attempts to describe real biological systems based on theoretical principles of
metapopulation dynamics have revealed that population spatial structure exists dong a
continuum (Harrison 1994; Hansson e t al. 1995; Hanski and Gilpïn 1997; Thomas =d
Kunin 1999). Degrees of rnetapopulation structures include: mainland-island systems -
considered as source-sink populations of conspecifics, separate systems - where
conspecific populations are completely isolated fYom one another, patchy systems - a
continuous population extending over multiple habitat patches, and classic systems -
involving independent populations capable of interaction (Harrison 1994). With such a
broad range of scenarios, populations of al1 species likely exist within this fiamework at
an appropriate temporal or spatial scale. Based on the preceding inference of population
structure, 'classic' metapopulation dynamics may best descnbe W: srnirhii dynamics and
distribution between bogs in this region over a broader temporal scale, while more patchy
rnetapopulation structure likely exists between points within bogs over a shorter temporal
scale.
Movement c m be broadly classified into two behaviourally distinct types;
migratory and maintenance. Maintenance represents movements for feeding,
reproduction, or cover. A generd pattern for mosquitoes is considered to be a migration
flight (if expressed) shortly after emergence and before females are repmduc tively active
( S e ~ c e 1976). If W. smithii usually expresses a longer, migration behaviour, our
recaptwe experiment has underestimated the movement potential of the species, but has
adequately estimated the range of its maintenance moves. The potential for longer, un-
detected migration movements exists. However, the maximum move distance recorded
for W. smithii was half the extent of the re-sampling grid, suggesting that the physical
ability of the organism limited its dispersal distance. In addition, incidental obsel-vations
of adult smithii in flight uidicate it is a weak and erratic flier (Bradshaw 1983; pers.
obs.). Likely, W. smithii does not move long distances, except in unusual (perhaps wind
aided) conditions, and might move further when the density of conspecifics reaches
threshold levels. These infkequent, long-distance movements might be s a c i e n t to
maintain metapopulation dynamics among local populations restricted to individual bogs.
Further studies exploring density dependence and long-distance movement could be
performed using various marking techniques (for example Giemsa stain, Kleckner and
Bradshaw 199 1) and M e r genetic work (sensu Istock and Weisburg 1987).
The movement data were m e r explored in the context of natural history and
systematics. The pattern of distribution of JK srnithii larvae fiom the release line infers
the species does not congregate in a mating s~varm, common to many species of
mosquitoes, and that females mate in the vicinity of the plant fiom which they emerge.
Corroborating morphological evidence shows that male W. smirhii have no physical
modifications for swarrning, and that their antemae dif5er only slightly fiom the fernale's
while more sensilla on male antennae is characteristic in other species (McIver and
Hudson 1972).
The dispersal behaviour of mosquitoes has been studied extensively because of
their propensity as vectors of disease. Malaria-control operations have studied anopheline
mosquitoes (Diptera, Culicidae, Tnbe Anophelini) extensively and report movement
potential of between one and ten kilometers. Wyeomyia smithii is classified within the
Tribe Culicinï (Diptera, Culicidae, Culicini, Group Sabethes), with species of Aedes
(Group Aedes) and CzrZex (Group Culex). A mark-recapture study of A. cornmunis
reported a maximum move of 1600 m (Joslyn and Fish l986), whiie a study of A. rzrsticus
in Gemany concluded that snow-melt mosquitoes tend to remain within 50 m of their
breeding sites (Schafer et al, 1997). Culex annulirostris moved up to 9000 m in an
Australian study (09Donnell et al. 1992). The recapture rate in this experiment was
relatively high (3.7%) for insect studies, suggesting that observed distances were
representative of typical move distances. Thus, the variation in the movement potential of
similarly-sized mosquitoes seems quite broad within the tribe and genera, and is likely
related to habitat requirements. Strong habitat selection by W. smithii for S. purpzrrea
may have resulted in selection for decreased flight abilities, enforced by the lethality of
intervening territory (forest) among subpopulations (bogs) (Tstock and Weisburg 1987),
and slow change or infrequent disturbance (e-g., succession or fire) within bogs.
In summary, understanding movement of organisms is an important step towards
understanding the dynamics of populations and ecosystems. Here, the movernent
potential of W. srnithii was used to indicate relevant spatial scales for M e r study of
individual and population dynamics. In addition, the study determined that simple
diffusion models can adequately describe the movement of W. smithii, thus facilitating
future avenues for modeling the dynamics of this species mathematically.
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Mogi, M. and Molay, J. 1980. Distribution of Wyeornyia srnithii (Diptera, Culicidae) eggs in pitcher plants in Newfoundlmd, Canada. Trop. Med. 22: 1 - 12.
OYDonnell, M.S., Berry, G., Carvan, T- and Bryan, J.H. 1992. Dispersal of adult females of Cdex annulirastris in GrifTith, New South Wales, Austrdia. J. Am. Mosq. Control Assoc. 8: 159- 165.
Okubo, A. 1980. Some examples of animal diffusion. In: Diffusion and Ecologicd Problems: Mathematical Models. Springer-Verlag, New York.
Price, R.D. 1958. Notes on the biology and laboratory colonization of Wyeornyia srnithii (Coquillett) @iptera:Culicidae). Can. Ent. 90:473-478.
Searle, S R , Casella, G. and McCuIloch, C.E. 1992. Variance Components. John Wiley and Sons, Inc, New York.
Service, M.W. 1976. Mosquito ecology. Field sampling methods. Applied Science Publishers, London.
Schafer, M., Storch, V., Kaiser, A., Beck, M. and Becker, N. 1997. Dispersal behavior of adult snow melt rnosquitoes in the Upper Rhine Valley, Germany. J. Vector Ecology 22: 1-5.
Thomas, C.D. and Kunin, W.E. 1999. The spatial structure Ecol. 68:647-657.
Turchin, P. 1998. Quantitative Analysis of Movement. population redistribution in animals and plants. Sunderland MA.
of populations. J. of Anirn.
Measuring and modelhg Simauer Associates, Inc.
Turchin, P. and Thoeny, W.T. 1993. Quantifj4ng dispersal of southern pine beetles with mark-recapture experiments and a diffusion model. Ecol. Applic. 3 : 18% 198.
Venables, W.N. and Ripley, B.D. 1996. Modem applied statistics with S-PLUS. Springer-Verlag New York, Inc. New York.
WilIiams, E.J. 196 1. The distribution of larvae of randomly moving insects. Aust. J. Biol. Sci, 12598-604.
Chapter 2. Movement potential of Flefclrermjia_fZefclreri (Diptera: Sarcophagidae): implications for the study of populations.
Introduction
Plant-insect communities are inieresting ecological systems due to the tight
interaction between pairs of species (Feeny 1976; Futuyma 1983). In the pitcher plant
(Sarraceniapurpurea) inquiline community, three species of fly, Wyeomyia smithii,
Metriocnemus knubi and Fletcherimyiafletcheri, are obligately related to the plant for
larval developrnent, adding three-fold complexity- Heard (1994) has coined the term
"resource chah commensalism" for this local-level l a r d community structure within the
leaves of S. purpurea, meaning that the behaviour of one species facilitates resource
acquisition of the other, with no benefit or h m to itself. At a larger spatial scale,
interaction of a comuni ty of adults of the rnosquito, W. smithii, the midge, M. knabi,
and the sarcophagid, F. fletcheri exists. Though the three species use the same resource
for larval development, distribution of adults, and thus population structure, is potentially
quite different due to unique life history strategies and habitat requirernents of each.
A valuable tool in quantitative analysis of communities is to lump together
species as an approach to simplieing phenomena and generalizing patterns of species
response (Levin 1992). However, it is as important to know what detail to ignore as it is
to know what detail to include Cudwig and Walters 1985). In other words, outstanding
characteristics of organisms can suggest unique processes and should be noted and
explored. Morphologically, F. flefcheri is lârge in cornparison to W. smil'hii and LM knabi.
Behavioural differences include the movement of F. fletcheri larvae fiom the S. purpurea
leaf to the surrounding Sphagnum spp. moss for ovenuintering as pupae (Forsyth and
Robertson 1975), and the use of S. purpurea flower heads by adults for roosting and
mating (Krawchuk and Taylor 1999; Appendix One). These char~cteristncs suggest that
individual assessrnent of component species of the tightly linked pitcher plant community
may yield significant dzerences in distribution and strategy of organisrrns in the system.
A mark-recapture study was designed to estirnate the movernent wotential of F.
fletcheri. These data were used to compare movement estimates with thobse derived in a
previous experiment for W. smithii, and to hypothesize how population s:tructure might
differ between the two species as a resuit of differences in this process.
Methods
Field procedure
The bog used for the F. fletcheri mark-recapture experiment was chosen for the
abundance of flowering purpurea plants it supported and its accessibiility. A recapture
grid was marked across the six ha bog using geo-referenced (Trimble Surveyor TDCI,
Trimble Inc. California) identification flags (n=l14) placed at each sam:_ple plant, chosen
as the closest flowering S. purpurea plant (hereafter plant or flower) to a standardized 25
m interval grid. At the centre of the bog, a 20 m2 zone contained 22 floweing plants
which were checked at three-day intervais, and used as the capture-mark area.
Aduits were marked and recaptured while roosting in flowerheadls (see Krawchuk
and Taylor 1999; Appendix One). The subjects were found by placing cl handheld aerial
insect net over the plant, pinching it closed around the base of the flawer's stalk and
manipulating the flower through the net such that the contents could be viewed. If a
sarcophagid was observed, the flower was shaken gently until the fly fell into the aerial
net nie nies were reshained by holding the thorax between the thumb and index finger
and a two-wing code unique for each census day was applied to the wings using a Sharpie
waterproof marker. Marked individuals were placed back on or in the flower fkom which
they were taken,
A c e m s of the entire grid took place between 0500 and 0700 hrs on eight
occasions between 8 JuIy and 28 July 1999. The flowers were checked for roosting adult
F. fletcheri using the net method described, above. If F. fletcheri were present, the view
was manipulated to determine if the wings were marked. The location of re-sighted,
marked individuals was recorded, and a straight line distance between this location and
the center of the capture-mark area was calculated using Pathfhder Pro GPS software
(Trimble, Inc. California).
Calcuiation of movement potential
The same diflbion equation could not be fit to these data as were fltted with the
K smithii data (Chapter One) since incidental observations made up more than haLf of
the re-sightings (Le., the entire trapping grid was not sampled on every occasion which
marked F. fletchen were observed). Instead, diffusion rate was estimated using a
procedure for individual mark-recapture data outlined in Turchin (1998), where D is a
mo vement measure of m2/t ime interval:
where x = the iength of move, and t = the duration for the move. D was calculated using
the distance moved per day for each capture (i.e., distance/days since marking) as x, and
assigned e l for al1 mcves (e-g., one day). .
Sirnilar to the general statistical descnptors of W. smithii movement in Chapter
One, the mean, variance, maximum, and minimum move distances were cdculated. Since
t h e was explicitly measured throughout the experiment, the mean time (in days)
between captures, daily mean move distance, and the relationship between move distance
and time were also calculated.
Results
The diffusion rate was estimated to be 114 rn2/day. The square root of this
measure produces a one-dimensional daily rate of movernent of 11 dday . There was no
relationship between move distance and the time elapsed since initial capture (r2 = 0.02,
n=9, p=0.7). Simple details of the experiment were tabuiated to iIlustrate general trends
of the data (Table 2-1). A cornparison between movement measures f?om F. fletcheri and
W. srnithii indicates an order of magnitude difference in their movernent potentiai (Table
2-1).
Table 2-1. A summary and cornparison o f information fiom field collection and
diffusion modelling used to estimate F. fletcheri and W. smithii (Chapter One) movement
potential.
Variable F. jletcheri W. smithii Source Number rnarkedkeleased 35 840 from release experiment Number recaptured 9 37 fiom release experiment Maximum net move distance (m) 184 Mean move distance (m) 34 Mean move distance per day 12
83 from release experiment 1 O fiom release experirnent n.a. kom release experiment
Mavimum time betwèen captures (days) 5 n.a. fiom re1ease experiment - -
Mean time between capm& (days) 3 n.a. frorn release exbenment Diffusion rate !14m2(-lldday) O.17m/ from dif is ion equation
generation
Discussion
The calculated diffusion rate per day (Table 2-1) from the modei of a tempordly
explicit, uncorrelated random walk corroborated with movement values calculated fiom
standard statistical procedures of the field data. This suggests the simpie equation could
adequately describe the magnitude of F. fletcheri movement potential within the scale of
a bog. nie calculated movement potential of 11 4 mL per day (diffusion rate) implies that
a dynamically synchronized population of F. fletcheri exists within the confines of a bog
- men a very large one. Further, movement between discrete bogs would be more
fiequent than with W. srnithii, whose mean observed move distance was 10 m over the
entire recapture period (difision rates, D, are not directly comparable between W. srnithii
and F. fletcheri due to diffèrent modeling procedures; Chapter One). In addition, the
results fiom the F. fleicheri mark-recapture experirnent show no relationship between
move distance and time, M e r implying that F. cfletcheri is a strong nier capable of
baversing the entire bog with ease. An observed movement distance can be a result of
landscape structure rather than an animal's maximum movement ability in mark-
recapture studies (Porter and Dooley 1993; Kindvall 1999). The maximum move distance
in the experùnent was recorded at the edge of the bog (and our re-sampling grid),
suggesting that this distance was imposed by bog structure, not by the ability of F.
fletcheri to continue moving. Alternatively, individuais might also remain in the vicinity
of a S. purpurea flower for extended time periods for mating and roosting if nectar
sources are located nearby to maintain energy stores.
The relative difference in body size between W. smithii (3 mm) and F. fletcheri
(7.5 mm) is substantial enough to suggest that the latter could make longer, more directed
moves. Though these two species share the same habitat, the Sphagnum spp. bog, and are
obligate to the same ovi/larviposition site, S. purpurea, their observed move distances
differ rnarkedly. This suggests that the parallel difference in movement potential and
body size is fbrther expressed as a difference in population spatial structure. An
interactive relationslip between animal body size (or body-mass) and landscape structure
has previously been suggested to structure ecosystems across temporal and spatial scales.
This relationship implies that changes in landscape structure may affect animals in
different ways, according to animal size and the spatial grain of the habitat (Holling
1992). Furthemore, Roland and Taylor (1997) have demonstrated that four parasitoid
insects responded to anthropogenic forest fragmentation at four different spatial scales
which corresponded to their relative body sizes. A neutral density-configuration response
of F. cfletcheri at the bog scale (Chapter Three) supports this conjecture that inter-bog
movement does not restrain population persistence, whereas a negative response was
detected for the smaller, W. srnithii, suggesting an effect of increased bog isolation on
population persistence.
References
Feeny, P. 1976. Plant apparency and chernical defense. In: Wallace, J. and ManseIl, R. (eds) Biochernical interaction between plants and insects. Am. Rev. Phytochem. 1O:l-40.
Forsyth, A.B. and Robertson, R.J. 1975. K reproductive strategy and larval behavior of the pitcher plant sarcophagid fly, BIaesoxiphafletcheri. Can. J. 2001. 53 : 174- 179.
Futuyma, D. J. 1983. Evolutionary interactions among herbivorous insects and plants. In: Dutuyma, D. J. and Slatkin, M. (eds) Coevolution. Sinauer, SunderIand, Massachusetts, U S .A.
Heard, S.B. 1994. Pitcher-plant rnidges and mosquitoes: a processing chah cornmensalism. Ecology 75: 1647- 1660.
Kolling, C. S. 1 992. Cross-scale morphology, geometry, and dynamics of ecosystems. Ecol. Monogr. 62:447-502.
Kindvall, O. 1999. Dispersal in a metapopulation of the bush cricket, Metrioptera bicolor (Orthoptera: Tettigoniidae). J. Anim. EcoI. 68: 172- 185.
Krawchuk, M.A. and Taylor, P.D. 1999. Roosting behaviour by FZetcherimyinfIetcheri (Diptera: Sarcophagidae) in Sarracenia purpztrea (Sarraceniacea). Can. Ent. 13 1 :829-830.
Levin, S.A. 1992. The problem of pattern and scaie in ecology. Ecology. 73 : 1943 - 1967. Ludwig, D. and Walters, C. J. 1985. Are age-structured models appropriate for catch-
effort data? Cm. J. Fish. Aquat. Sci. 42:1066-1072. Porter, J.H. and Dooley, J.L. 1993. Animal dispersai patterns: a reassessment of simple
mathematical models. Ecology 78:243 6-2443. Roland, J. and Taylor, P.D. 1997. Insect parasitoid species respond to foresr structure at
different spatial scales. Nature 3 86:ï 1 0-7 1 3. Turchin, P. 1998. Quantitative Analysis of Movement. Measuring and modeling
population redistribution in anirnals and plants. Sinnauer Associates, Inc. Sunderland MA.
Chapter 3. The relative importance of habitat structure changes within a nested hierarchy of spatial scales for three species of insects.
Introduction
Ecologicd pattern and process are manifest within a hierarchy of spatial scales
across the landscape (Kotliar and Wiens 1990; Levin 1992). Simply put, process (such as
movement or recruitment) drives patterns of distribution, and structure (such as amount
of suitable habitat) constrains them (Levin 1992). The relationships found between
structural properties of habitat and population or community responses at various scales
suppoa the concept that the physical environment influences ecosystem dynarnics (e.g.,
Bender et al. 1998; Trzcinski et al. 1999). Recent interest in broad, ecosystem and
landscape-Ievel spatial heterogeneity and its underlying mechanisms is illustrated by
studies of "lumpiness" in ecological systems (e-g., Holling 1992), density-area
relationships (Andrén 1994; Bowers and Matter 1997; Bender et al. 1998; Comor et al.
2000; Matter 2000), metapopulation dynamics (Harrison 1994; Hanski 1999), effects of
Iandscape fragmentation (McGarigal and McComb 1995; Robinson et al. 1995; With and
Crist 1995; Fahrig 1997; Villard et al. 1999; Trzcinski et al. 1999; Drolet et al. 1999) and
ecosystem rnodeling (e.g., Walters et al. 2000). Yet, a cross-scale translation of local-
level patterns attributed to habitat requirements, home range size, and community
interaction to organization at these broader spatial scales has proven to be challenging
(Addicott et al. 1987; Wiens 1989; Holling 1992, Wiens et al. 1997, Comor et al. 2000).
Explicitly hierarchical studies have begun to adàress this challenge (Senft et al.
1987; Rukke and Midtgaard 1998; Bowers and Dooley 1999; Turner et al. 1999; Kehler
and Bondrup-Nielsen 1999; Fauchald et al. 3000; Nielsen and Ims 2000) by relating a
variety of responses (e-g., predation or incidence) to measures of structure (e-g., prey or
habitat). Results fiom these works suggest that correlations among variables at small
scales rnay change in magnitude, disappear or even change sign when the scale is
extended (e-g., Wiens 1989; Fuhlendorf and Smeins 1999).
Ecologists fiequently refer to habitat structure parsimoniously using two
variables: the amount of habitat (quality of area) and its configuration (spatial pattern,
geometry, isolation) (Taylor et al. 1993; but see Hanski and Ovaskainen 2000). In the
context of habitat loss and fragmentation, the importance of these two components for
population persistence has been explored both theoretically (Fahrig 1997, 1998) and
empirical ly (Andrén 1994; McGarigal and McComb 1995; Bender et al- 19%; Trzcinski
et ai. 1999; Villard et al. 1999). The amount of habitat has repeatedly been claimed to be
the primary concem for conservation (McGarigal and McComb 1995; Bender et al. 1998;
Fahrig 1998; Drolet et al. 1999; Trzcinski et al. 1999). However, the importance of
configuration (e.g., fiagmentation, nearest neighbour distance) may be far fiom negligible
(Villard et al. 1999) for some species (McGarigal and McComb 1995; Fahrig 1998;
Rukke and Midtgaard 1998; Villard et al. 1999) at some spatial and temporal scales (e-g.,
metapopulation dynamics (Hanksi 1999)). In particular, it has been s h o w that there are
thresholds where the relative impact of configuration increases drarnatically as the
amount of habitat decreases (Andrén 1994; Fahrig 1997; Trzcinski et al 1999; Villard et
al. 1999). Since habitat destruction and fiagrnentation is of global concem (Margules and
Pressey 2000), there is an urgent need to clan@ the importance of these two broad
measures of habitat structure in conservation strategies.
Previous studies e x p l o ~ g these two structural concepts (amount and
configuration of habitat) are limited because they examine either single spatial scales
(McGarigal and McComb 1995; Fahrig 1997, 1998; Drolet et al. 1999; Trzcinski et al.
1999; Villard et al. 1999)' hierarchical scales with low replication (Nielsen and Ims 2000)
or without the discrete treztment of amount and configuration at each scale (Andren
1994; Fabrig 1997; Rukke and Midtgaard 1998; Bowers and Dooley 1999), and (or) have
only a single species' response (Rukke and Midtgaard 1998; Bowers and Dooley 1999).
These limitations provide a template for designing a more comprehensive assessment of
organism response to habitat structure.
Since movement between resources is critical to habitat use and population
survival (Taylor et al. 1993) i t is important to consider another element of structure:
connectivity. Landscape connectivity is the degree to which the landscape facilitates or
impedes movement among resvurce patches (Taylor et al. 1993). Since the environment
between suitable patches of habitat is often heterogeneous, this cari influence an
organism's ability to reach and therefore use this habitat, in addition to the amount or
configuration of habitat. The degree of between-patch ("matrix") heterogeneity will
dictate the influence of this structural measure on distribution. Cntical thresholds in
connectivity have been s h o w to differ for species with varying habitat specialization and
dispersal range (With and Crist 1995). Thus, this additional structural measure will Vary
in its importance and influence on organism distribution across spatial or temporal scales.
With these concepts in mùid, three main ideas are explored here. This chapter
addresses the relative importance of amount and configuration of habitat in a hierarchical
analysis of the distribution of W- smithii, M. knubi and F. fletcheri, al1 of which have the
same discrete habitat requirement, namely S. purpurea. Second, it compares responses to
habitat structure between the three species of insects. Third, this chapter explores the
influence of habitat texture (as a variable influencing comectivity) on distribution at a
single spatial scale.
Methods
Field methods
Census of W. smithii, M. knabi and F. fletcheri larvae in S. purpurea Ieaves was
conducted in the Main River Watershed (UTM: 55 14000N 478000E Zone 2173 lOkm
outside the border of Gros Morne National Park in western Newfoundland, Canada (Fig.
1-1). As described in the general introduction, this area of boreal forest is composed of
discrete patches of bog withui mature coniferous forest and softwood scmb (Fig. 1-2).
Data were collected during two sampling sessions, the f ~ s t between 6-27 June and the
second between 17-25 August, 1999. These two periods were chosen to census over-
wintered larvae before pupation and emergence as adults (first sample in June), and
distribution of the current year's larval cohort (second sample in late August). W. snzithii
normally have clutch sizes of between one (Mogi and Mokry 1980; Heard 1994a) and
three eggs (Bradshzw 1983): F. fletcheri deposit a single iarva into each pitcher (Forsyth
and Robertson 1975), and M. knabi fernales consistently lay eggs in large numbers
(Heard 1994a). Because of this consistent ovi/larviposition behaviour, Iarval abundance
was used as an index of adult distribution and density for al1 three species. Since F.
fletcheri over-winter in Sphupum spp. moss, they were only counted in the second
(August) sample.
Field sampling was designed to coilect response data - larval counts within a leaf
for each of three insect species (Table 3-1) - as well as a nested suite of environmental
variables from a local to landscape scale (Table 3-2). Hierarchically nested levels of
sampling included leaf, plant, point, bog, landscape.
Table 3-1. A surnmary of l a r d sarnpling effort by spatial scale and sampling period.
Spatial scaIe Sample 1 Total samples Sample 2 Total samples 6-27 June 17-25 August
Landscapes 2 2 2 2 Bogs in a landscape 20 40 20 40 Patches in a bog 2-8 202 2-8 202 Plants in a patch 3 606 3 606 Leaves in a plant 3 1817 3 1817
Landscapes one and two were chosen since each 8 km2 area provided variability
in arnount and configuration of bogs. Landscape one contained 7 % bog and landscape
two contained 20 % bog (thus decreased distance between bogs and/or larger bog areas).
These values were calculated using SPANS GIS software (Intera Tydac Technologies,
Nepean, Ontario, Canada) analysis of Forest Resource Inventory Maps of the area. A
balanced sample of bogs varying in size and nearest neighbour distance were chosen with
M e r information fkom 150 000 topographical maps of the area and GIS maps provided
by Corner Brook Pulp and Paper Ltd. (Fig. 1-2).
At each of these chosen sampling bogs, structural attributes representing arnount
and configuration of habitat were measured at four scales (leaf, plant, point, bog) (Table
3-2, variables are followed by their short forms in srnall caps; Figure 3-1). The amount of
habitat (Le., patch size) was estimated at each scaie so that larval samples were associated
with: a leaf volume (PONOL), plant size (LEAVES), point density (PTDENS), and bog area
(BGAREA) and abundance (BGABUN; estimated number of plants within a bog).
Configuration of habitat was estimated at three scales so that individuai sampies were
associated with: a distance to nearest plant neighbour (NNEIGH), index of distance to
point neighbour (PTCONF), distance to next nearest bog neighbour (BGNIU'EI). In addition,
habitat texture was measured at the point scale as an influence on habitat connectivity
(CONNEC) -
The amount, configuration and connectivity of habitat, and additional
environmental covariates were measured as follows (Table 3-2). Bog area (BGAREA) and
distance to nearest neighbouring bog (BGNNEI) were measured using SPANS GIS
software on geo-referenced 150 000 aerial photos fiom August 1985. The structure of
the area has changed little since then. Abundance (BGABUN) of purpurea plants in a bog
were estimated by multiplying bog area by the mean density of the bog'; two density
transects (details befow). Bogs were considered to be discrete if they had more than 15 m
of high scrub or trees between them.
Sample points were chosen pseudo-randornly in each bog. A point is a two meter
radius sarnpling circle. Smail bogs contained between two and four points, the largest bog
contained eight points. Each point was placed no M e r t h m 20 m fYom the bog edge to
minimize edge effects since plants and their inhabitants appear to be influenced by their
distance fiom the bog edge? attributed to exposure to winds and decreased snow cover
(Heard 19946; Miner 1999), or the thickness of the Sphagnurn spp. The locations of
Table 3-2. Summary of structural variables used in the multi-scale sarnpling of ÇV.
smithii, M. knabi and F. fletcheri in leaves of S. purpurea of the Main River study area of
Newfoundland. Structural variables used to estimate amount of habitat are indicated by
'A', configuration by 'C', and texture by 'T'. Response variables are indicated by 'R'.
Additional variables descnbed in this table were included as habitat descriptors in glms
or ornitted due to collinearity.
Spatial Description of variable Variable Range Mean Range Mean scale name Sample Sarnple sample sample
One One Ttvo Two
plant
point
bog
leaf potential volume (mL) A POTVOL 1.049.0 12.0 0.5-48.0 10.0 actual volume (mL) ACTVOL 0-27 2 0-40 6 detritus (categorical) DETRiT 0-3 2 0-3 2 midpes (larval count) R MIDGES 0-90 9 0-65 6 mosquitoes (larval count) R MOSQUI 0-24 1 .O 0-3 7 1.5 sarcophagids (larval count) R SARCOP NA NA O or Z 0.05 length of leaficm) LENGTH 0.5-17.2 8.7 1.1-79.0 8.4 leaf width at hood (cm) WlDTH 0.5-5.0 2.2 0.4-6.7 2.1 nurnber of leaves A LEAVES 3-47 7 2-3 2 7 distance to nearest neighbour (m) C NNEIGH 0.02-3.5 0.5 0.03-2.7 0.4 count within 2m radius of centre A PTDENS 2-62 14 2-62 14 density (categoncal) PTDENC High, NA High, NA
Low Low bog density C PTCONF 0.14- 0.69 O. 14- 0.69 (mean of 2 transects; lm') 0.54 0.54 texture (categot-kal) T CONNEC High, NA High, NA
Low Low distance to edge (m) DIST2E 0-16 3 0-16 3 area (km') A BGAREA 0.0020- 0.039 0.0020- 0.039
O. 17 O. 17 abundance (density * area) A BGABUN 1700- 19360 1700- 19360
77540 77540 nearest neighbour (km) C BGNNEI 0.020- 0.19 0.020- 0.19
0.68 0.68 landscape LANDSC 1 o r 2 NA 1 or2 NA
Figure 3-1. A visual summary of study design and variables representing amount and
configuration of habitat. A) bog configuration (distance to nearest neighbour); 8) bog
area; C) two transects counting plant density within a bog (an index of point
configuration); D) density of plants at a point (amount of habitat); E) plant configuration
(distance to nearest neighbouring plant) for each of three plant samples at each point.; F)
amount of habitat at the plant scale (nurnber of leaves), the three youngest leaves were
sarnpled on each plant.
points were picked if their area had a miaimum of three healthy plants (at minimum three
healthy leaves capable of containing fluid). Each point was flagged and geo-referenced
using a Trimble Surveyor TDCl (Trimble Inc., California). These points were chosen to
complete a bdanced sampling of S. purpurea density (PTDMC) and texture (height of
surrounding vegetation; CONNEC) categorically as follows: high vegetation- high density;
high vegetation-low density, low vegetation-high density, low vegetation-low density.
Point density was considered high if more than six S. purpurea plants were found within
a two metre radius circle of the centre (point area), and low if less than six. Explicitly,
texture is the height of surrounding vegetation within the point area. For example, a point
among tall grasses or shnibs was considered high, while a point among only Sphagnzm
spp. was considered low. The texture of the point may influence the connectivity of
habitat. The structure of each sample point was M e r described by a continuous variable
of plant density within the point area (PTDENS). An index of the configuration (PTCONF) of
point clusters of S. purpurea in bogs was estimated fiom counts of plants within two, 1
m-wide transects which crossed each bog between randomly chosen points wherein
higher densities of plants = closer clusters.
The nearest three plants to the centre of each point were chosen for sampling. The
number of leaves per plant (LEAVES) and the distance and bearing to the nearest
neighbouring plant (NNEIGH) was recorded. The three healthiest leaves were carefblly
removed fiom each plant. A healthy leafwas considered if it had no rips and was
succulent, with a large enough opening for successful navigation by the three study
species. Liquid contents of each leaf were poured into a 20 rd, screw top vial. The vial
and the leaf were then wrapped in a plastic sample bag marked with the bog, point, plant
and leaf number. AIl samples were processed within 24 hrs of collection.
Processing involved the measurement of leaf contents fiom the vile including:
abundance of mosquito (MOSQUI), midge (MIDGE) and sarcophagid (SARCOP) larvae,
arnount of detritus (DETEUT), and the actual volume of fluid (mL) i? the leaf (ACTVOL).
Potential volume (mL) of the leaf (POTVOL) was calculated by measuring the amount of
water it contained when it was filled to capacity. Thorough census of leaf contents was
ensured by slicing the leaf open, and flushing the remaining contents into a sampling tray
for identification (sensu Nastase et al. 1995; Miner 1999). Other morphological
meâsurements of each leaf included: leaf length (LENGTH), hood width (WIDTH) and
condition.
Sarnples Etom the second census were collected fiom the sarne locations as the
first census whenever possible. When necessary, the nearest sultable location for a new
point was sarnpled.
Statistical methods
The statistical analysis of the relationship between habitat structure and insect
distribution consisted of two steps. The first step was the removal of variation in response
data fiom more local effects using generalized linear models (ghs). The second step was
to determine the relationship between these residuals (remaining variation) and measures
of structure at higher scales using mixed linear models (lmes). Generalized linear models
were built in S-PLUS 2000 (MathSoft, Inc. Seattle, Washington) to isolate, and remove
the effects of field-measured variation (Table 3-2) on larval counts of the three species of
insects. For example, at the bog scale, a glm was first built wherein counts of larval W-
srnithii were response variables, and all variables measured at the leaf, plant and point
scale (Table 3-2) were inchded as predictors. ResiduaIs fiom this mode1 were then used
as response measures to bog structure, whereas at the point scale, the gim only included
variables fiom the leaf and plant level, and residuals were then used against measures of
point structure.
A Quasi-likelihood family (link = log, variance = mu) was used in al1 cases since
the count data of W. smithii and M knabi larvae were over-dispersed in a log-linear
(Poisson) regression model and F. fletcheri data were under-dispersed using a logistic
(Binomial) regression model (response data were one or zero). Quasi-likelihood
estimation is commoniy used to estimate regression relationships k r data kvith
incomplete knowledge of the error disîribution of the response variable (McCullagh and
Nelder 1 99 1 ; MathSoft Inc. 1999), allowing the user to define both the lulk and variance
function to estimate regression coefficients.
The residuals of these Quasi-Iikelihood g h s for W. srnithii and M knabi were
normally distributed, allowing the use of linear rnixed models (Ime; Pinheiro and Bates
2000) to explore their relationship with habitat structure. The variation in adult density
may be attributed (statistically) to a mixture (hence "mixed" model) of both random
(associated with experimental units drawn at random fkom a population (MathSofi Inc.
1999)), and fixed (associated with an entire population, or with repeatable levels of
experimental factors (MathSoft Inc. 1999)) effects. Here. fixed effects were the amount,
configuration and comectivity of habitat, and random effects were associated with the
hierarchically nested smcture of sampling (a plant within a point within a bog within a
landscape),
A slightfy different process of analysis was used for FJZetcheri since bimodal
distribution of residuak Çom glm models made the ime an inappropriate next step. A
pseudo rnixed-effects model was created using a glm and fkst including a factor effect for
each sarnple at each level of scde (ive., a unique factor for each plant, or bog) to mimic
random effects (Pinheiro and Bates 2000) of a mixed model. The point factor effects
were significant, indicating differences between individuai points unassociated with
structural variables. The landscape, bog and plant factors were insignificant effects and so
were not included here for simplicity. Thus, this method addresses the pertinent issue of
generalized models of multiple mixed effects data with nested structure. A similar
statistical method resulting in the same analytical structure for di three species would be
the use of a generalized linear mixed model (such as the macro GLMMK in SAS).
Results
The glms indicated significant relationships between the abundance of larvae and
the chosen suite of environmental variables (Tables 3-3, 3-4,3-5). This variation was
removed fkom each lower spatial scale before rnodelling the influence of amount,
configuration or texture of habitat on insect distribution. Leaf-level variables LENGTH,
W ~ T H and point-bel variabies DISTE and PTDENC were not used in analysis since they
were collinear with other structural variables.
For W. smith ii and knabi, mked h e m modds ( h e ) were used on glm
residuals of larval counts to infer the relationship between adult density and habitat
structure. S irnilarly , levels of structure were added sequentially to the glrn for F. fletcheri.
The results show that response changes with spatial scaie and diffen between species
(Tables 3-4,3-5,3-6; Fi,pre 3-2). The inclusion of interaction terms in rnodels did not
significantly improve their fit, thus no evidence for significant interactions between
amount and configuration of habitat was detected. The texture of habitat at the point scale
was significant for ail three species (Tables 3-43-5,3-6), where a negative relationship
indicates higher density at points with lower surrounding vegetation, and a positive,
higher density in higher vegetation.
Table 3-3. Summary of glm output for W. smifhii. Significant relationships between
variables and Iarval abundance are in bold. The direction of coefficients is indicated as
'coef . Incremefitally higher levels of scale were included in the g h s according to the
scale being fit with successive linear mixed models me).
Scale Variable Sample 1 Sample 2 Deviance Residual P(F) coef Deviance Residual P(F) coef
d f d f NULL 5760 1816 7438 1816
leaf POTVOL 873 1815 <0.001 + 1020 1815 <0.001 + ACn'OL 246 1814 ~0 .00 1 + 56 1814 -=0.001 + D ETRIT 43 1811 0.01 + 93 1811 -=0.001 + MIDGES 5 181U 0.2 + 2 1810 0.6 + SARCOP NA NA NA NA 21 1809 0.03 + AW0L:POTVOL 181 1804 <0.001 110 1803 <O.Oo 1 ..
plant NNEIGH 0.2 1809 0.8 + 1 1808 0.7 -+
LEAVES 77 1805 <O.OO 1 - 83 1807 <O.OO 1 - point CONNEC 181 1807 43.00 1 - 61 1806 <O.OO 1 -
PTCONF 0.1 1806 0.9 44 1805 0.002 + PTDENS 24 1805 0.01 + 1770 1804 <0.001 + Dispersion 3.8 4.6 Parameter Residual 4128 1804 5770 1803
Table 3-4. Summary of glm output for M. knabi. Significant relationships between
variables and Iarval ablmdance are in bold, The direction of coeEcients is indicated as
'coef . uicrementally higher levels of scde were included in the glms according to the
scale being fit with successive linear mixed models (lme).
Scale Variable Sample 1 Sarnple 2 Deviance Residual P(F) coef Deviance Residual P(F) coef
d f d f NULL 14811 1816 13015 1816
Ieaf POTVOL A W O L DETRfT MOSQU SARCOP ACI7rOL:POTVOL
p lant W E I G H LEAVES
point CONNEC PTCONF PTDENS
Dispersion 7.0
18 15 18 14 181 1 1810 1809 1803 1 SOS 1807 1806 1803' 1804
Parameter ResiduaI II614 1804
Table 3-5. Summary of glm output for the relationship between variables and larval
abundance of F. fletdieri. The mode1 includes as.factor@ointid) to milnic a mixed-mode1
procedure. Generalized linear modek fit effects sequentidly, thus significance of effects
are calculated in the order they are included.
Scale VariabIe Deviance Residual P(F) coeff d f
NULL 578 1816 as.factor(pointid) 230 1615 eo.001
leaf POTVOL 1 1614 O. 15 + ACTVOL 2 1613 0.008 - DETRIT 7 1610 (0.00 1 +- MIDGES 5 1609 eo.00 1 - LMOSQUI 4 1608 <O.OOI + ACTV0L:POTVOL 0.1 1601 0.6 -
plant NNEIGH 2 1607 0.006 - LEAVES 2 1606 0.006 -
point PTDENS 0.1 1605 0.5 - PTCONF 0.2 1604 0.8 - CONNEC 2 1603 0.005 -
bog BGABüN 0 1602 >O -99 - BGAREA 0 1601 >0.99 + BGNNEI 0 1600 >O -99 i-
Dispersion 0.3 Parameter Residual 321 1600
Table 3-6. Summary of output f?om the mixed-effects models (he s ) representing the
relationship between W- smithii density and the amount, configuration and connectivity
of habitat at multiple spatial scdes.
Scale VariabIe Sam~le 1 Sam~le 2 ~ o e f t-value P(F) ~ o e f t-value P(F)
plant AMOUNT CONFIGURATTON
point AMOUNT CONFIGURATION CONNECTIVITY
0% AMOUNT (area) AMOüNT (abundance) CONFIGURATION
Table 3-7. Summary of output from the mixed-effects models (lmes) representing the
relationship between M. knabi density and habitat structure at multiple spatial scales
Scale VariabIe Sample 1 Sarnple 2 Coef t-value P(F) Coef t-value P(F)
plant AMOUNT O. 1 3.8 0.0006 0.2 4.1 <0.0001 CONFIGURATION 0.3 O -4 0.6 0.01 0.02 0.9
point AMOUNT -0.04 -1.5 0.1 -0.01 -0.6 0.5 CONFIGWWTION -1.0 - 1.9 0.07 -0.4 -1 .O 0.3 CONNECTNITY 2.5 4.0 0.0001 2.1 5.0 <0.0001
bof? AMOUNT (area) 7.5 1 0.3 -5.2 -0.7 0.5 AMOUNT (abundance) <0.000 1 0.7 0.5 C-0.0001 -0.3 0.8 CONFIGURATION 1-8 0.8 0.5 5.5 2.9 0.006
leaf plant point bog Spatial scale (m)
Figure 3-2. The direction and scale of significant relationships between W. smithii, A4
knabi, and F. JZetcheri density and the structural variables amount and configuration of
habitat at four nested levels of spatial scaie. In general, amount of habitat influences
density at relatively finer, and configuration at broader spatial scales, though species
respond at slightly different absolute scales correspondhg to evolutionarily divergent
attributes such as body size andor movement potential. Squares represent a significant
relationship with amount of habitat, circles represent a significant relationship with
configuration of habitat. The directions of response denved from coefficients of gims
(leaf) and lmes (plant, point, bog) are indicated as + or - within each symbol. Grey fil1
indicates a rnargindly sianificant effect. Statistical values are found in Tables 3-3 to 3-7.
Discussion
The data suggest a significant relationship between the distribution of W. smithii,
1M. knnbi, and F. fletcheri and the effects measured to represent arnount, configuration
and connectivity of habitat. The direction and magnitude of these relationships differ
between spatial scales within and between study species. Here, larvd samples one and
two are treated as joint indicators of relationships with habitat structure since their
direction rernained consistent even though levels of significance differed between the two
samples. In contrast with the findings of Andrén (1994), no evidence for interactions
between the arnount and configuration of habitat were detected to suggest thresholds
where the influence of configuration increased with decreasing amount of habitat at any
scaie, for any species in this system.
The W. srnirhii models reved a change in the direction of density response to
amount of habitat between the leaf (potential volume), plant (number of leaves) and point
scales (point density). At the bog scale, importance flips fkom amount to configuration
(distance to nearest neighbour) of habitat (Figure 3-2). Support for these density-
arnouddensity-configuration patterns is provided by movement/behaviour studies, Field
observations (Bradshaw 1983; pers. obs) describe females visiting leaves of multiple S.
purpurea plants in an area (point). Variance components analysis (Chapter One) irnplies
that a female selects a leaf within a plant for independent oviposition events, but moves
within a group of pIants (point) over her lifetime. For an individual, the point measure is
an appropriate scale of a habitat patch (sensu Addicott et aI. 1987). This study suggests
that local dynamics at a point scale are positively influenced by amount of habitat, for
example through individual recmitrnent and/or survivorship. The negative plant-lcveI
reIationship with amount of habitat (more Ieaves per plant = fewer Iarvae per leaf) was
not a result of decreased prey-base (detritus per leaf; sensu Farkas and Brust 1985) and is
likely a result of (unmeasured) constraint forcing local populations to function below
their apparent carrying capacity (Istock et al. 1975), such as overwintering mortaliv.
Release-recapture experiments of W. smithii (Chapter One) indicace that
movement occurs between the point and bog scale (1 0-100 m) and genetic work suggests
panmixis within a bog, rather than between bogs (Istock and Weisburg 1987). Thus, for a
population of individuals a patch of habitat (or ecological neighborhood) Iikely
encompasses mdtiple pokts, or an entire bog. A 'patchy' metapopulation structure may
operate between points within bogs. The negative density relationship with bog
configuration (distance to nearest neighbour) suggests that population dynamics respond
to rates of emigratiodimmigration with neighbouring bogs, and implies that a classic
metapopulation-type system (Hanski 1999) may operate at this bog scale.
The data corroborate with work by Fahrig (1998) where the circumstances under
which the breaking apart of breeding habitat (with no habitat loss, therefore a change in
configuration) would affect population persistence were predicted using a spatially
explicit simulation mode1 of fragmentation. One of these (narrow set of) conditions was
that the average between-generation movement distance of the organism be roughiy one
to three times the expected nearest distance between suitable (population) breeding sites.
Bogs within the boreai forest of western Newfoundland are separated by areas of
softwood scrub or mature softwood forest as narrow as 25 m and extending to 2000t m.
Based on Fahrig's (1998) prediction, the short movement potential (maximum of - 90 m)
of W. ssmithii (Chapter One) relative to actual distances between bogs (population
breeding sites) suggest that the configuration of bogs within this nahirally heterogeneous
boreai forest should impact population persistence.
The M. knabi data similady suggest changes in the significance of density
response to amormt and configuration of habitat. Aithough no movement information is
available for M kzabi, adults are srnaller than W. smithii and statistical inference of
movement potential using variance cornponents andysis (unpublished data; Miner 1999)
suggests that individuals have limited rnovement potential and cluster around plants,
wtiereas W. smithii cluster around the Iarger scale of points (Chapter One). In the VCA,
peaks of unusually high variance are suggested to indicate scales at which between-group
differences are especially large, inferring the scale of natural aggregation or patchiness
(Greig-Smith 1952, 1979). If we match relative scales, W. srnithii and A4 knabi respond
positively to amount of habitat locally, (point and plant scafes, respectively), and
configuration at broader scales.
Configuration at the point scale is marginally, negatively, significant in sample
one, and at the broadest, bog scale, there is a positive density-configuration relationship
for M. knabi for sample two. The former suggests metapopulation-type dynamics at the
point scale, the latter indicates that there may be some higher-level regional process at
work, which we can detect for the smallest species (M knabi) but not for the two larger
species. Biologically, the fluctuation in these configuration responses between samples
one and two might be temporal, and attributed to the unusual life cycle of M. knabi. The
life-cycle is described to encompass three generations every two years (Paterson and
Carneron 1982), where one cohort emerges in early and one in late summer. Heard
(1994a) describes Newfoundland M. knabi phenology differently, insisting there is a
single emergence event (stnctly univoltine). In this study we observed events more like
the 'two in three' described by Paterson and Cameron (1982)- As a result the sarnples are
collected fiom two independent cohorts within the same area and these aggregations may
respond to structure slightly differently. Further information on M. knabi movement
potential a d o r genetic variation would assist in interpreting these patterns.
The relationship between habitat structure and F. fletcheri density is strongest at
the smallest scales, and no bog-scale effects were detected. Configuration and amount of
habitat at the plant level are both significantly, negatively correlated to F. fletcheri
abundance, and could be associated with natural history attributes of the fly. Unlike W-
smirhii and knabi, whose larvae overwinter in S. purpwea and pupate to emerge as
adults afker the fourth instar, F. fletcheri Iarvae move out of the plant and pupate in the
surrounding Sphagnum spp. moss where they oveminter and from which they emerge as
adults (Forsyth and Robertson 1975). Information about emergence and adult behaviour
is scant. However, it is known that adult F. fletcheri roost overnight within the flower
heads of S. purpurea and use them as a mating arena (Krawchuk and Taylor 1999).
Potentially, it is beneficial for pupae to emerge near ne ighbohg plants for protection as
tenerais. This link is speculative since amount of habitat at the point scale has no
relationship to larval abundance. Female F. fletcheri Iarviposit a single offsprllig in a
purpurea leaf. If competition for resources between individuals exists (e.g., for available
flower heads) at spring emergence of tenerals, a plant with fewer leaves may provide a
less cornpetitive patch than one that could support the development of multiple
individuals in its many leaves.
Mark-recapture of F. fletcheri indicated fiequent cross-bog movement (Chapter
Two) indicating that inter-bog rnovement would be more common than with the smaller
statured W. smithii or M. knabi Correspondingly, both point and bog codiguration did
not influence F. fletcheri density, suggesting that strong movement potential can
overcome structural constraints imposed by the boreal forest matrix. This implies that
individual bogs are not independent components of a metapopulation (that may exist at
an even broader spatial scale).
A lack of evidence for "threshold" behaviour il this system that would
demonstrate an increased influence of configuration with decreased arnount of habitat,
could be attributed to a number of factors. For example, the imposed levels of scale may
be inappropnate to the phenornenon for these three species, or sampling methodology
may not be adequate to resolve more cornplex interactions in the system. Very small
habitat patches might help illustrate a compensatory response between arnount and
configuration in the bog system. However, this study did not sample extremely small bog
patches, as they were not discernable fiom GIS maps at the beginning of the study. It
seems logical that configuration rnight become more important in scenarios where habitat
is less abundant. However, previous studies proposing tfüs threshold (Andrén 1994;
Fahrig 1997; Bender et al. 1998) might also be illustrating a change in structural
relationships as we have demonstrated, with increased spatial scale. This should be
explicitly tested or controlled.
Vegetation texture at a point was measured as a factor influencing habitat
connectivity and had a significant influence on the density of al1 three study species. A
higher W. smithii density in areas with lower surrounding vegetation suggests that these
areas were more easily accessible to ovipositing females, or that thermal microclimate as
a result of increased plant exposure may be preferable in this northem, boreal system
m g s o l v e r 1979). In contraçt to W- smithii, areas with lower texture exhibited decreased
density of M knabi suggesting that either movement away fiom plants was increased by
Iower surrounding vegetation either actively, or passively as a result of wind-throw; or
that rnicrociimate provided by areas of high vegetation provided better habitat for M.
knabi. The texture between plants at a point was also significant to F. fletcheri density.
Since F. fletcheri has the potential to move across an entire bog easily (Chapter Two), the
influence of vegetation height suggests that identification of andor movement to plants
was facilitated by lower vegetation.
These relationships highlight the importance of considering "matrix", (or
cccontrast", "context", "texture") between patches of habitat as a structural measurement,
especially if it appears pertinent to the study organism based on natural history
information. For simplicity, some spatially explicit studies and rnodels often focus on
patch characteristics (With and Crist 1995; Fahrig, 1997) at the expense of matrix
variables. While this parsimony is sometimes valid, the inclusion of additional variables
could prove important in predicting organism response (Hiebeler 2000). In our system,
connectivity was only measured at the point scale. Its inclusion at the Ieaf or plant scale
did not appear Iogical (or quantifiable). The boreal forest between study bogs was equally
heterogeneous across the entire study site. However, a sirnilar study comparing hamested
(where clear-cuts exist as the matrix) and naturaI landscapes might suggest an effect of
connectivity at the bog scale.
Scaling issues have been addressed in ecology throughout this decade (Kotliar
arid Wiens 1990: Levin 1992; Wu and Loucks 1995). This study uriiquely illustrates how
inter- and intra-specific response to habitat structure is inconsisient within and across
scales, even when species are strictly linked to the same resource. The importance of
amount and confiavation of suitable habitat on organism density changes with increasing
spatial scale. The fkequency and scaie of these changes is different for various organisms
and can be linked to scales of process, such as movement. Only when pattern is scaled to
process do these similarities begin to emerge. As postulated, there is no single
appropriate spatial (or temporal) scale at which to study nature cev in 1992), or even
individual species. With this in rnind, techniques for study integration such as meta-
analysis must diligently focus on equivalent levels of spatial and temporal scale explicitly
when combining data from various studies (Bender et al. 1998; Connor et al. 2000).
Accordingly, conservation issues can not be addressed at either a single scale or with a
single structural antidote.
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paradigm shift in ecology. Quart. Rev. Biol. 70:439-466.
Synopsis
The overall significance of this study c m be considered - in keeping with the
theme of the thesis - at two different scales. 1 consider the f i s t scale to be population and
cornmunity ecology, nested within the broader scale of conservation biology. Here, 1
have devetoped a clearer understanding of the population dynamics of W. smithii, M
knabi and F. fletcheri through the exploration of their movement potential, and their
relationship with habitat structure. In the context of a cornmunity, I have illustrated that
the members of this inquiline community exhibit unique processes (movement) and
patterns, despite their similar obligate habitat requirement, the larval 'nursery' within S.
purpurea leaves. This work adds to the phenornenal amount of Soma t ion that describes
the life history and ecology of this inquiline community. This volume of is needed to
understand local-level dynamics and provide a solid base fkom which to build studies at
Iarger scales exploring regional and ecosystem dynamics.
At a broader, landscape scale the significance of this study is its demonstration of
the variation in the response of species using the sarne microhabitat to the structure of
their shared environment. This variation exists among spatial scales and species.
However these relationships appear to scde to processes, such as movement. Likely,
temporal variation in response adds further complexity. We found that the amount of
habitat is most relevant at local scales, and the configuration at 'popülation' scales. It
would be interesting to determine whether this trend exists across a broader range of taxa
and ecosystems. Since most native organisms would be sirnilady adapted to the naturally
patchy landscape, population structure of these insects may heIp predict how the region's
other flora and fauna might react to habitat structure and changes to it, as a result of
forestry or natural disturbance. Sirnilarly, since this study was performed in a 'natural'
environment, the change in response as a result of varying connectivity (e-g., f?om
forestry) between habitat patches at a number of scales seems to be a logical next step.
Further, it is ememely important to begin recognizing the @oteiitially vat ) spatial extent
of structure that influences organism distribution.
This study was developed and implemented within the Gros Morne Greater
Ecosystern, an area of boreal forest including Gros Morne National Park and the
surrounding landscape. Since this landscape is currently the issue of a debate between
conservation/ecological integrity and economic gaidforestry, it seems suitable, necessary
in fact, to place the results of this study into this context. It is inevitable that the area will
be harvested within the next few years, but forestry operators of the area are willing to
discuss ecologicdly sensitive cutting patterns. Certainly, the concepts that were
investigated with this thesis provide ideas and mornentum for conservation principles
well beyond the scope of the pitcher plant community. Why not test these results - a
hypothesis is better than no plan at all. 1 w-ould suggest the choice of a few target species,
of which our knowledge of process (such as movement and habitat requirements) is well
developed (e.g., birds). Using our knowledge of these species, and an interactive dialogue
with the harvest planners, it rnight be possible to design cut patterns that test the influence
of arnount and configuration at local and Iandscape scales (scaled to be relevant to the
target species) in an altered ecosystem.
Appendk 1. Roosting behaviour by Fletcfzerimyiafletcfzeri @iptera: Sarcophagidae) in Sarracenia piirpurea (Sarraceniacea)
The flute-shaped Ieaves of the pitcher plant Sarraceniapurpurea L., are fluid-
filied microhabitat rich in invertebrate diversity (Bradshaw 1983; Heard 1994; Hardwick
and Giberson 1996; Harvey and Miller 1996; Miller et al. 1994). They are the obligate
Iarval habitat for F'i'efcherimyiafletcheri (Aldrich) (Forsyth and Robertson 1975). Most
Literature reports of F. Jetcheri present information o d y on larval life history and
population dynamics (Fish and Hall 1978; Hardwick and Giberson 1996). Forsyth and
Robertson (1975) state anecdotdly that they observed adults feeding on flowers and other
nectar sources within their study area. We believe that our observations represent the first
report of adult F. Jletcheri roosting within the flower heads of the pitcher plant.
On 3 July 1 998, during a survey of pitcher pIant Ieaves for Iarval F. fletcheri
conducted in boglands of the Long Range Mountains of Gros Morne National Park
(49E3SYN, 58E5OYW), Newfoundland, one of us (MAIS) fust observed, at about 1900,
adults of F. fletcheri using the flower heads of S. purpurea as roosting sites. A survey
conducted immediately after that observation revealed that 51 flower heads were
occupied by F. fletcheri. Most had one or two occupants; three plants held four, four, and
six F. fletcheri, respectively. The distribution of individuals was non-random (clumped)
cX2 = 1 1.07; P<O.OOl; n=75 flower heads). Where two flies were observed, they were on
opposite sides of the flower head, facing opposite directions with no apparent interaction.
In two plants containing greater than two flies, several pairs were mating (one fly on top
of another, with abdominal tips touching). In one plant with four occupants no mating
was observed. Fuaher evening censuses were undertaken between 10 and 27 July in 20
bogs ranging fiom low coastal zones to rock barren highlands. Occupation rates varied
f?om 3/135 to 43/167 flower heads, usudy with a single fly per flower head. By August,
we no longer observed F. fletcheri roosting with any regularity, which we expect was due
to seasonal cessation of adult activity.
Observations of individual fly behaviours at pitcher plant flowers revealed the
following general patterns. Fletcherimyiafletcheri were usually observed landing on the
sepals of the flower (on the upper surface, because the flower head is nodded) shortly
before dusk (approximately 1800-1900; 2 h prior to sunset). Within 30 min of dighting,
individuals would walk into the bowl of the flower. (The shape and structure of the
flower, with its "nodding" head, provides an urnbrella-like enclosure.) When left
undisturbed they appear to remain within the flower head for the night. In a prelirninary
study, 10 occupied flower heads were marked one evening and al1 10 were still occupied
by F. fletcheri when rechecked prior to 0900 the following morning.
Between 0700 and 0900 the foIIowing morning (2 h after sunrise), roosting F.
fletcheri would move fkom the bowl of the flower ont0 the outer face of the sepds. M e r
10-30 min of basking, individuals would fly from the flower, afier which they could not
be followed. When individuals were disturbed fiom the flower heads, they dropped to the
ground and flew only short distances, alighting on and gradually ascending other
vegetation in the area. One inciividual was observed to drop kom the flower head to the
rrround and fly directly to a neighbouring flower head roughly 30 cm distant. C
Fletcherimyiaflercheri were never observed within the flower heads between 2 h after
sunrise and 2 h prior to sunset.
Why individuals roost within the flower heads is unknown. A total of 3 h over
three evenings were spent sweeping, beating, and perusing other vegetation in various
boglands. Fletcherimyiaflefcheri was never found occupying foliage other than the
pitcher plant. Thus, it appears as though the behaviour is uniquely associated with pitcher
plants. Individuals were observed apparently feeding (head buried in pollen on stamen)
on pitcher plant pollen only once, so the plant does not appear to provide a primary food
resource. As well, F. fletcheri continued using the flower heads even as the plants lost
petals and starnen. The flower head shape rnay encapsulate a microclimate different fkom
the surroundhg environment, thus protecting individuals from wind, rain, and changes in
temperature. It may also provide a refuge from predators. One likely explanation,
especially given our observations of mating, is that the flower heads provide assembly
site and perhaps some king of cue for mating.
Multiple individuals of an unknown species of Coleoptera were observed in the
flower heads fkequently for a penod of 1 week, but no other insect species were obsenred
in the pitcher plant flower head so consistently or over the extended penod of time
recorded of F. flefcheri.
The roosting habit of F. fletcheri is interesting as an adult behaviour, even more
so because of the further, obligate association of its lava to the pitcher plant.
We thank Parks Canada and the Western Newfoundland Mode1 Forest for
financial support. We are grateful to M Holder, K Menchenton, J Miner, D Potter and D
Rogers of Agriculture Canada, Kentville. BE Cooper, Canadian National Collection
(CNC), Ottawa, verifïed the identification of voucher specimens. Vouchers have been
deposited with the CNC, Ottawa.
References
Bradshaw, W.E. 1 983. Interaction between the mosquito Wyeomyia smithii, the midge Mefriocnemus knabi, and their camivorous host Sarraceniapzvpurea. In: Frank, J.H. and Lounïbos, L.P. (eds), Phytotelmata: terrestnal plants as hosts of aquatic insect communities. PIexus, Medford, N.J.
Fish, D. and Hall, D. W. 1 978. Succession and stratification of aquatic insects inhabiting the leaves of the insectivorous pitcher plant, Sarracenia purpurea. Am. Nfidl. Nat. 99:172-183.
Forsyth, A.B. and Robertson, R.J. 1975. K reproductive strategy and larval behavior of the pitcher plant sarcophagid fly, BZaesoxiphafIetcheri. Cm. J. Zool. 53 : 174-1 79.
Hardwick, M.L. and Giberson, D.J. 1996. Aquatic hsect populations in transplanted and natural populations of the purple pitcher plant, Sarraceniapurpzcrea, on Prince Edward Island, Canada- Cm. J. Zool. 74: f 956- 1963.
Harvey, E. and Miller, T.E. 1996. Variance in composition of inquiline communities in leaves of Sarracenia purpurea L. on multiple spatial scales. Oecologia 1 O8 :562- 566.
Heard, S.B. 1994. Pitcher-plant rnidges and mosquitoes: a processing chah cornmensalism. Ecology 75: 1647- 1660.
Miller, T., Cassill, D-, Johnson, C., Kindell, C., Leips, J., McInnes, D., Bevis, T., Mehlman, D. and Richard, B. 1994. Intraspecific and interspecific cornpetition of Wyeomyia smithii (Coq.) (Culicidae) in pitcher pIant communities. Am. Midi. Nat. 13 1:136-145.