Download The Value of Animal Behavior in Evaluations of Restoration Success

OPINION
The Value of Animal Behavior in Evaluations of
Restoration Success
Catherine A. Lindell1,2,3
Abstract
Animals are key members of ecosystems, contributing to
processes like pollination, seed dispersal, and herbivory.
Incorporating measures of animal behavior into evaluations of restoration success will provide critical information that is not available from animal species composition
and richness estimates derived from the documentation of
species presence and absence. Behavioral studies will (1)
allow comparisons of the habitat quality of target and reference sites based on behaviors that have fitness consequences for organisms; (2) provide valuable information
about reasons for differences in habitat quality; (3) identify critical resources that make a site suitable or not for
Introduction
A recent issue of Restoration Ecology has a special section
devoted to the measurement of biodiversity (Zerbe &
Kreyer 2006) and indices of biodiversity are commonly
used to evaluate the success of restoration projects (RuizJaen & Aide 2005). Although faunal components of ecosystems have often been overlooked when assessing the
success of restoration efforts (Halle & Fattorini 2004),
determining indices of animal biodiversity, usually species
composition and richness, is becoming more common
(e.g., Jansen 2005; Ottonetti et al. 2006; Summerville et al.
2007). This is a welcome development in that animals are
key players in ecosystem function. Arthropods are important herbivores and pollinators (e.g., Coley & Barone
1996; Balvanera et al. 2005) and affect decomposition processes (e.g., Chapman et al. 2003). Birds disperse seeds of
numerous plant species (e.g., Wunderle 1997), serve as
pollinators and decomposers (Sxekercioğlu 2006) and mediate herbivory levels on plants by foraging on insects (e.g.,
Greenberg et al. 2000). Mammals disperse seeds (e.g.,
Bollen et al. 2004) and influence decomposer populations
(e.g., Botes et al. 2006). Mollusks and fish have important
effects on the abundance and reproductive success of
1
Department of Zoology, 203 Natural Science Building., Michigan State
University, East Lansing, MI 48824, U.S.A.
2
Center for Global Change and Earth Observations, 218 Manly Miles
Building., Michigan State University, East Lansing, MI 48823, U.S.A.
3
Address correspondence to C. A. Lindell, email [email protected]
Ó 2008 Society for Ecological Restoration International
doi: 10.1111/j.1526-100X.2008.00389.x
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Restoration Ecology Vol. 16, No. 2, pp. 197–203
particular species; and/or (4) provide information on the
mechanisms through which species contribute to ecosystem functions. When resources for the evaluation of restoration success are available, practitioners should carefully
consider the costs and benefits of the different variables
they could quantify. In some cases, it may be more important to compare the behavior of one or a few critical animal species that contribute to ecosystem function rather
than try to document the presence or absence of all
species.
Key words: animals, behavior, ecosystem function, habitat
quality, restoration success.
other trophic levels (e.g., Frederiksen et al. 2005; Vaughn
et al. 2007).
Species composition and richness estimates, however,
provide only part of the picture when assessing the responses of animal species to restoration efforts. Behavior
is a critical component of the contribution of animals to
restoration processes, yet is rarely quantified in evaluations of restoration success. I argue that, in many cases,
behavioral sampling in both restoration and reference
sites will provide valuable information with which to
assess the success of restoration efforts. Documentation of
behavior will (1) allow comparisons of the habitat quality
of target and reference sites based on behaviors that have
fitness consequences for organisms; (2) provide valuable
information about reasons for differences in habitat quality; (3) identify critical resources that make a site suitable
or not for particular species; and/or (4) provide information on the mechanisms through which species contribute
to ecosystem functions.
Limitations of Assessing Restoration Success with
Presence/Absence Data
Successfully restored sites should contribute to individuals
being able to reproduce at a rate that allows their population to replace itself, that is, maintain a net reproductive
rate equal to or greater than 1. The mere presence of
individuals in a site is not strong evidence that the site contributes positively to individual reproductive success and
population replacement (Aldridge & Boyce 2007). However, presence/absence data are usually the cornerstones
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Animal Behavior and Restoration Success
of species composition and richness estimates. Previous
studies have demonstrated that individuals use habitats in
which their reproductive rates are not great enough for
population replacement (e.g., Burke & Nol 2000; Hels &
Nachman 2002). The most obvious situations in which
presence does not reflect the suitability of a habitat are
ecological traps. Ecological traps occur when individuals
prefer a habitat in which they actually have lower fitness
than habitats that are not preferred (Robertson & Hutto
2006). Ecological traps may be particularly common in
human-modified landscapes (Battin 2004).
Measurements of variables directly related to the likelihood of population replacement will generally be very useful in evaluating the success of restoration efforts. For
example, nest success and nest density are strong influences
on population replacement in birds (e.g., Pidgeon et al.
2006). However, documenting reproductive success does
not explain why individuals in one site have higher reproductive success than individuals in other sites. This missing
information may be key to determining components of restoration efforts that are adequate and those that are not. In
addition, although some sites undergoing restoration are
large enough to provide all the resources necessary for
individuals to carry out their daily and seasonal activities,
including reproduction, many are not. In these cases, restoration sites may be contributing resources like food or protection from predators but not breeding resources like den
or nest sites (e.g., Kus 1998). Thus, even if it were possible
to assess individuals’ reproductive success by tracking them
to breeding areas outside the restoration sites, it would be
difficult to calculate the contribution that the food or protection offered in the restoration site made to the individuals’ reproductive success and to population replacement.
Finally, studies to document reproductive success are
extremely labor intensive and may yield small sample
sizes, particularly for species of special concern (Pejchar
et al. 2005). Incorporating studies of behavior into assessments of restoration success will help address these issues.
Successful Restoration: A Behavioral Perspective
Behavioral patterns often reflect habitat quality (e.g.,
Vaughan et al. 1996; Johnson 2000; Persson & Stenberg
2006). In addition, an individual’s fitness, that is, the genes
it contributes to the next generation (Alcock 2001), is often
closely linked to rates and/or outcomes of behaviors (e.g.,
Good et al. 2000; Persons et al. 2002; Vos & Hemerik 2003;
Watson et al. 2007). Recent work indicates that even shortterm behavioral decisions, such as when to leave a food
patch, reflect the quality of an individual’s habitat and are
linked to potential fitness. For example, fish in high-quality
habitats departed from patches of food sooner (i.e., had
a higher ‘‘giving up density’’) than fish in low-quality habitats. This variation in behavior explained more than 50%
of the variation in fish size, which is positively correlated
with potential reproductive output (Persson & Stenberg
2006). Thus, there are strong links between behavior, habi-
198
tat quality, and potential fitness (Olsson et al. 2002). Restoration ecologists can take advantage of these links by
quantifying behavior to assess the relative quality of restoration sites and to identify reasons for differences in quality. Quantifying behavior also provides information on
potential drivers of species presence or absence, such as the
availability or lack of important resources. Finally, documenting behavior can identify how species contribute to
ecosystem function and will be particularly useful in cases
where determining reproductive success is not feasible
because of logistical or financial constraints and for sites
that are not used extensively for reproduction.
Comparing Habitat Quality
Variations in foraging behavior can indicate differences in
food availability with higher food availability generally indicating higher quality habitat. Numerous studies with birds
and fish have documented higher foraging rates at sites
where food is in greater abundance compared with sites
with lower food abundance (e.g., Repasky 1996; Delestrade
1999; Shepherd & Boates 1999; Marchand et al. 2002;
Wellenreuther & Connell 2002; Kilgo 2005). Observations
of foraging-related behaviors can also provide useful information about how differences in habitat quality vary for different species. Two insectivorous bird species in Panama
foraged in coffee fields and forest but only one showed a
lower foraging rate in coffee, indicating the coffee was lower
quality habitat for only this species (Pomara et al. 2003).
Anti-predation behavior is also closely related to habitat
quality. Pronghorn antelope exhibited greater vigilance
rates in habitat near roads, where cars were a common
cause of mortality, than further from roads (Gavin &
Komers 2006). Increases in predation risk and associated
anti-predation behavior can lead to decreases in foraging
efficiency (e.g., Metcalfe et al. 1999; Kotler et al. 2004;
Orpwood et al. 2006). For example, at greater distances
from safe habitat, wild goats spent more time being vigilant
and showed higher giving up densities than goats closer to
escape habitat (Hochman & Kotler 2007). Thus, in cases
where anti-predation behavior and foraging behavior are
shown to be strongly correlated, it may be possible to focus
on just one of these behaviors in efforts to evaluate the relative quality of reference and restoration sites.
To use behaviors such as those described above and in
Table 1 as indices of restoration success, it is important to
develop a priori predictions about the relationship between
the behavior and habitat quality, based on previous empirical work and theory. For example, the relationship between
foraging rate and habitat quality may vary between taxonomic groups. Whereas high foraging rates for birds usually indicate high-quality habitat (e.g., Delestrade 1999;
Shepherd & Boates 1999; Kilgo 2005), mammalian browsers
and grazers may increase food intake rates to compensate
for poor quality of available food during some seasons
(e.g., Taillon et al. 2006). As another example, recent theory predicts that individuals of solitary species should have
Restoration Ecology
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Restoration Ecology
Spool-and-line
Telemetry
Birds, mamm
Amph, arth, birds, mamm,
fish, rept
Amph, arth, birds, fish,
mamm,
moll, rept
Amph, mamm
Amph, birds, fish, mamm,
moll, rept
Amph, birds, fish, mamm,
moll, rept
Amph, arth, birds, fish,
mamm,
moll, rept
Amph, birds, fish, mamm
Low
Low to Moderate
Observations
Field experiments
High
Telemetry
Low
Low to moderate
Mark-recapture
Observations
High
Low
Low
Moderate
Low
Low to moderate
Telemetry
Observations
Field experiments
Tuberville et al. (2005), Garla et al.
(2006)
Brashares & Arcese (2002), Walters
et al. (2002)
Ricketts (2004), Fink et al. (in press)
Holl (1998), Zahawi & Augspurger
(2006)
Lemckert & Brassil (2000)
Winker et al. (1995), Baldwin et al.
(2006)
Grimm & Paill (2001), Wauters et al.
(2005)
Able et al. (2005), Ortega et al. (2006)
Matthysen et al. (1995), Rouquette &
Thompson (2007)
Wellenreuther & Connell (2002),
Pomara et al. (2003)
Gavin & Komers (2006)
Kotler et al. (2004), Hochman &
Kotler (2007)
Slabbekoorn & Peet (2003), Sun &
Narins (2005)
Luck (2003), Stauss et al. (2005)
Marsh & Borrell (2001), Yang (2006)
References
a
Groups are those I considered most likely to be of interest in restoration studies and include amphibians (amph), arthropods (arth), birds, fish, mammals (mamm), mollusks (moll), and reptiles (rept). Groups listed
are those for which the behavior is regularly measured.
b
Financial costs associated with equipment, not labor.
Social behavior (group size,
tendency to group)
Visitation rate (in the context
of pollination or seed
dispersal)
Amph, arth, birds, fish,
mamm, rept
Arth, birds
Arth, birds
Low to moderate
High
Observations
Site searches,
observations
Mark-recapture
Amph, arth, birds, mamm
Vocalizations (frequency,
rate)
Provisioning behavior
Den/nest/oviposition site
selection
Movement, dispersal
(distance, likelihood of)
Territory/home range size
and overlap
Site fidelity (turnover rates)
Low to moderate
Recordings
Birds, fish, mamm
Birds, mamm
Low
Anti-predation (vigilance or
allocation of time)
Observations
Arth, birds, fish, mamm
Relative Costb
Foraging rate
Methods
Groupsa
Behavior
Table 1. Behaviors that could be quantified in studies to evaluate restoration success. References provide information on methods, but were not necessarily conducted in restoration
contexts.
Animal Behavior and Restoration Success
199
Animal Behavior and Restoration Success
larger home range sizes in areas with low habitat quality compared with areas of high habitat quality (McLoughlin
et al. 2000; Wauters et al. 2005). However, these patterns
may vary with factors such as the sex of the individuals
(Lurz et al. 2000). Thus, it is important to consider the
species and the context in the design and interpretation of
behavioral studies conducted to assess restoration success.
Determining Reasons for Differences in Habitat Quality
Behavioral observations can provide information that is
critical to determining why sites differ in quality. Blue tits
in Germany, for example, fledged fewer offspring per nest
in poor-quality habitat, a coniferous woodland, compared
with high-quality habitat, a deciduous woodland (Stauss
et al. 2005). Documentation of this difference, however,
provided no information on the reasons for the difference.
By also observing parental provisioning behavior, including the distances parents traveled to find food, investigators were able to determine that parents in the poorquality habitat had to travel further per provisioning trip.
The number of provisioning trips parents could make in
the poor-quality habitat reached an asymptote and limited
the number of fledglings produced per brood below that of
the high-quality habitat (Stauss et al. 2005). This type of
information can inform restoration efforts by identifying
how habitat composition and structure influence behaviors
that are critical to survival and reproductive success.
Identification of Important Resources
Behavioral studies demonstrate which resources are important to species. For example, studies of giant barred
river frogs in New South Wales revealed that individuals
stayed within 20 m of streams and used two types of
daytime shelter locations with distinctive characteristics
(Lemckert & Brassil 2000). In Hawaii, an endangered
Hawaiian honeycreeper foraged primarily on one species
of native hardwood tree that can be grown in plantations
(Pejchar et al. 2005). The absence or presence of critical
resources in sites undergoing restoration may determine
the success of the restoration effort with regard to particular species. They may also indicate flaws in current restoration efforts. For example, despite the importance of
black locust and hackberry trees to birds in Illinois forests,
as demonstrated by behavioral observations, current techniques for savanna restoration in this area discourage the
growth of these tree species (Hartung & Brawn 2005).
Contributions to Ecosystem Function
The Society for Ecological Restoration states that an attribute of a restored ecosystem is that it ‘‘functions normally’’
(The Society for Ecological Restoration 2004). Behaviors
that provide functions critical to an ecosystem’s recovery
may vary with habitat and/or landscape characteristics that
can be considered in the design of restoration efforts. Several studies have demonstrated that bird behavior is influenced by restoration design, including the size of planted
200
patches (Zahawi & Augspurger 2006; Fink et al. in press),
the types of perches available (Holl 1998), and the tree species planted (Zahawi & Augspurger 2006; Fink et al. in
press). Variations in behavior are linked to variation in processes like seed dispersal that contribute to restoration success (Holl 1998; Zahawi & Augspurger 2006). Animal
behavior influences other processes that are critical to restoration success and ecosystem function including decomposition, herbivory, and pollination (Chapman et al. 2003;
Van Bael & Brawn 2005; Feldman 2006). The design of restoration projects may facilitate or impede the recovery of
these processes through effects on animal behavior.
Apportioning Resources to Behavioral Studies
Resources to evaluate the success of restoration efforts
are often very limited. Thus, when resources for evaluation are available, practitioners should carefully choose
variables that are likely to provide them with the greatest
amount of information. Although determining species
presence/absence and species richness are commonly measured and important in many cases, particular species
often play more significant ecological roles than others
and/or are of greater conservation concern than others.
For example, one or a few species may be particularly
important seed dispersers or pollinators in a system (e.g.,
Wenny & Levey 1998; Ricketts 2004). Thus, a more strategic use of resources in some cases may be to measure the
behavior of a few key species, rather than to try to comprehensively sample the presence of all species.
Methods used to quantify behavior vary in equipment
costs. Observations of foraging or vigilance behavior, for
example, could be incorporated into a study for a low
cost—in many cases, a pair of binoculars. At the other
end of the spectrum, the equipment necessary to document movement patterns with telemetry is very expensive.
Table 1 lists some of the behaviors that could be measured
in studies to evaluate restoration success and their relative
costs with regard to equipment.
Another cost of incorporating behavioral assessments
into restoration studies is finding or developing the expertise to conduct such assessments. Partnering with behavioral ecologists is one way for restoration ecologists to
gain access to this expertise (e.g., Fink et al. in press).
Another way is to take advantage of local amateur knowledge. Members of birding and nature clubs are often eager
to share their know-how about animal behavior with newcomers and, with some effort, it is not difficult to develop
observation skills that are sufficient to identify a few key
species and categorize their behaviors.
A final cost to behavioral assessments is the labor involved in conducting the studies. Quantifying most of the
behaviors in Table 1 would involve moderate to high labor
costs. A potential source of labor is volunteers. Volunteers
have been used successfully to gather data in animal conservation and/or monitoring programs in a number of
countries (e.g., Garnett et al. 1999; Gregory et al. 2005;
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Animal Behavior and Restoration Success
de Solla et al. 2006) and the Cornell Lab of Ornithology
currently has several programs that use volunteers to collect data on behavior (Cornell Lab of Ornithology 2008).
Given the strong interest many volunteers have in habitat
conservation (Weston et al. 2003), studies involving monitoring in restoration sites would be attractive. Administering volunteer programs is not effortless, but can produce
large quantities of useful data and involve local citizens in
science (West 2000). Volunteer labor will not work in all
situations, for example, in areas of the developing world
where people struggle to make a living.
Conclusions
Few previous studies have incorporated behavioral data
into assessments of restoration success (e.g., Holl 1998;
Brusati et al. 2001; Armitage et al. 2007). I argue that measurements of behavior should regularly be considered by
investigators as components of evaluations of success.
Quantification of behavior often will provide a better index
of the quality of a site than the simple presence or absence
of species and will provide insight as to why sites differ in
quality. Behavioral studies also will indicate resources that
are important to species. They will provide information as
to how species contribute to ecosystem function and how
these contributions vary with restoration design. Behavior
will often demonstrate the mechanisms through which the
attributes of restored ecosystems, including a characteristic
assemblage of species and a normally functioning ecosystem
(The Society for Ecological Restoration 2004), are realized.
Given the importance of restoration in a world with vast
areas of degraded lands (Lamb et al. 2005), it makes sense
to make the most of our limited resources by choosing the
most information-rich ways to evaluate restoration success.
Implications for Practice
Animals are key players in many ecosystem processes yet often receive little attention in evaluations
of restoration success.
d When the animal components of restoration efforts
are assessed, it is often with species composition and
richness estimates derived from presence/absence
data.
d Measures of animal behavior can compensate for
many of the limitations of presence/absence data by
providing information about why reference and restoration sites differ in quality, identifying critical resources for animals, and documenting how animals
contribute to ecosystem function.
d When resources are available to assess the success of
restoration efforts, behavioral studies should be considered as a potentially rich source of information.
d If practitioners choose to use animal behavior to
evaluate restorations success, they should carefully
develop testable predictions to guide the design,
analysis, and interpretation of such studies.
d
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Acknowledgments
I am grateful to Karen Holl, Richard Hobbs, Emily Morrison, and Rakan Zahawi for helpful comments on earlier
drafts of this manuscript.
LITERATURE CITED
Able, K.W., L.S. Hales, Jr., and S.M. Hagan. 2005. Movement and growth
of juvenile (age 0 and 11) tautog (Tautoga onitis [L.]) and cunner
(Tautogolabrus adspersus [Waldbaum]) in a southern New Jersey
estuary. Journal of Experimental Marine Biology and Ecology 327:
22–35.
Alcock, J. 2001. Animal behavior: an evolutionary approach. 7th edition.
Sinauer Associates, Inc., Sunderland, Massachusetts.
Aldridge, C.L., and M.S. Boyce. 2007. Linking occurrence and fitness to
persistence: habitat-based approach for endangered Greater SageGrouse. Ecological Applications 17:508–526.
Armitage, A.R., S.M. Jensen, J.E. Yoon, and R.F. Abrose. 2007. Wintering shorebird assemblages and behavior in restored tidal wetlands in
southern California. Restoration Ecology 15:139–148.
Baldwin, R.F., A.J.K. Calhoun, and P.G. de Maynadier. 2006. Conservation planning for amphibian species with complex habitat requirements: a case study using movements and habitat selection of the
Wood Frog Rana sylvatica. Journal of Herpetology 40:442–453.
Balvanera, P., C. Kremen, and M. Martinez-Ramos. 2005. Applying community structure analysis to ecosystem function: examples from pollination and carbon storage. Ecological Applications 15:360–375.
Battin, J. 2004. When good animals love bad habitats: ecological traps
and the conservation of animal populations. Conservation Biology
18:1482–1491.
Bollen, A., L. Van Elsacker, and J.U. Ganzhom. 2004. Relations between
fruits and disperser assemblages in a Malagasy littoral forest: a community-level approach. Ecology 20:599–612.
Botes, A., M.A. McGeoch, and B. J. van Rensburg. 2006. Elephant- and
human-induced changes to dung beetle (Coleoptera: Scarabaeidae)
assemblages in the Maputaland Centre of Endemism. Biological
Conservation 130:573–583.
Brashares, J.S., and P. Arcese. 2002. Role of forage, habitat and predation in the behavioural plasticity of a small African antelope. Journal
of Animal Ecology 71:626–638.
Brusati, E.D., P.J. Dubowy, and T.E. Lacher, Jr. 2001. Comparing ecological functions of natural and created wetlands for shorebirds in
Texas. Waterbirds 24:371–380.
Burke, D.M., and E. Nol. 2000. Landscape and fragment size effects on
reproductive success of forest-breeding birds in Ontario. Ecological
Applications 10:1749–1761.
Chapman, S.K., S.C. Hart, N.S. Cobb, T.G. Whitham, and G.W. Koch.
2003. Insect herbivory increases litter quality and decomposition: an
extension of the acceleration hypothesis. Ecology 84:2867–2876.
Coley, P.D., and J.A. Barone. 1996. Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics 27:305–335.
Cornell Lab of Ornithology. 2008. Urban Bird Studies (available from
http://www.birds.cornell.edu/programs/urbanbirds) accessed 18 January
2008.
Delestrade, A. 1999. Foraging strategy in a social bird, the alpine chough:
effect of variation in quantity and distribution of food. Animal
Behaviour 57:299–205.
de Solla, S.R., K.J. Fernie, C.G. Barrett, and C.A. Bishop. 2006. Population trends and calling phenology of anuran populations surveyed in
Ontario estimated using acoustic surveys. Biodiversity and Conservation 15:3481–3497.
Feldman, T.S. 2006. Pollinator aggregative and functional responses to
flower density: does pollinator response to patches of plants accelerate at low densities? Oikos 115:128–140.
201
Animal Behavior and Restoration Success
Fink, R.D., C.A.. Lindell, E.B. Morrison, R.A. Zahawi, and K.D. Holl.
Patch size and tree species influence the number and duration of
bird visits in forest restoration plots in southern Costa Rica. Restoration Ecology (in press).
Frederiksen, M., P.J. Wright, M.P. Harris, R.A. Mayor, M. Heubeck and
S. Wanless. 2005. Regional patterns of kittiwake Rissa tridactyla
breeding success are related to variability in sandeel recruitment.
Marine Ecology Progress Series 300:201–211.
Garla, R.C., D.D. Chapman, B.M. Wetherbee, and M. Shivji. 2006.
Movement patterns of young Caribbean reef sharks, Carcharhinus
perezi, at Fernando de Noronha Archipelago, Brazil: the potential
of marine protected areas for conservation of a nursery ground.
Marine Biology 149:189–199.
Garnett, S.O. Whybird, and H. Spencer. 1999. The conservation status of
the Spectacled Flying Fox Pteropus conspicillatus in Australia.
Australian Zoologist 31:38–54.
Gavin, S.D., and P.E.. Komers. 2006. Do pronghorn (Antilocapra
americana) perceive roads as a predation risk? Canadian Journal
of Zoology 84:1775–1780.
Good, T.P., J.C. Ellis, C.A. Annett, and R. Pierotti. 2000. Bounded hybrid
superiority in an avian hybrid zone: effects of mate, diet, and habitat
choice. Evolution 54:1774–1783.
Greenberg, R., P. Bichier, A.C. Agnon, C. MacVean, P. Perez, and
E. Cano. 2000. The impact of avian insectivory on arthropods and
leaf damage in some Guatemalan coffee plantations. Ecology 81:
1750–1755.
Gregory, R.D., A. van Strien, P. Vorisek, A.W. Gmelig Meyling, D.G.
Noble, R.P.B. Foppen, and D.W. Gibbons. 2005. Developing indicators for European birds. Philosophical Transactions of the Royal
Society of London B Biological Sciences 360:269–288.
Grimm, B., and P. Wolfgang. 2001. Spatial distribution and home-range
of the pest slug Arion lusitanicus (Mollusca: Pulmonata). Acta
Oecologica 22:219–227.
Halle, S., and M. Fattorini. 2004. Advances in restoration ecology: insights
from aquatic and terrestrial ecosystems. Pages 10–33 in V.M.
Temperton, R.J. Hobbs, T. Nuttle, and S. Hale, editors. Assembly
rules and restoration ecology: bridging the gap between theory and
practice. Island Press, Washington, D.C.
Hartung, S.C., and J.D. Brawn. 2005. Effects of savanna restoration on
the foraging ecology of insectivorous songbirds. Condor 107:
879–888.
Hels, T., and G. Nachman. 2002. Simulating viability of a spadefoot toad
Pelobates fuscus metapopulation in a landscape fragmented by
a road. Ecography 25:730–744.
Hochman, V. and B.P. Kotler. 2007. Patch use, apprehension, and vigilance behavior of Nubian Ibex under perceived risk of predation.
Behavioral Ecology 18:368–374.
Holl, K.D. 1998. Do bird perching structures elevate seed rain and
seedling establishment in abandoned tropical pasture? Restoration
Ecology 6:253–261.
Jansen, A. 2005. Avian use of restoration plantings along a creek linking
rainforest patches on the Atherton Tablelands, North Queensland.
Restoration Ecology 13:275–283.
Johnson, M.D. 2000. Evaluation of an arthropod sampling technique for
measuring food availability for forest insectivorous birds. Journal of
Field Ornithology 71:88–109.
Kilgo, J.C. 2005. Harvest-related edge effects on prey availability and foraging of hooded warblers in a bottomland hardwood forest. Condor
107:627–636.
Kotler, B.P., J.S.. Brown, and A. Bouskila. 2004. Apprehension and time
allocation in gerbils: the effects of predatory risk and energetic state.
Ecology 85:917–922.
Kus, B.E. 1998. Use of restored riparian habitat by the endangered Least
Bell’s Vireo (Vireo bellii pusillus). Restoration Ecology 6:75–82.
202
Lamb, D., P.D.. Erskine, and J.A. Parrotta. 2005. Restoration of degraded
tropical forest landscapes. Science 310:1628–1632.
Lemckert, F., and T. Brassil. 2000. Movements and habitat use of the
endangered giant barred river from (Mixophyes iterates) and the
implications for its conservation in timber production forests. Biological Conservation 96:177–184.
Luck, G.W. 2003. Differences in the reproductive success and survival of
the rufous treecreeper (Climacteris rufa) between a fragmented and
unfragmented landscape. Biological Conservation 109:1–14.
Lurz, P.W.W., P.J.. Garson, and L.A. Wauters. 2000. Effects of temporal
and spatial variations in food supply on the space and habitat use of
red squirrels, Sciurus vulgaris L. Journal of Zoology 251:167–178.
Marchand, F., P. Magnan, and D. Boisclair. 2002. Water temperature,
light intensity and zooplankton density and the feeding activity of
juvenile brook charr (Salvelinus fontinalis) Freshwater Biology 47:
2153–2162.
Marsh, D.M., and B.J. Borrell. 2001. Flexible oviposition strategies in
tungara frogs and their implications for tadpole spatial distributions.
Oikos 93:101–109.
Matthysen, E., F. Adriaensen, and A.A. Dhondt. 1995. Dispersal distance
of nuthatches, Sitta europaea, in a highly fragmented forest habitat.
Oikos 72:375–381.
McLoughlin, P.D., S.H. Ferguson, and F. Messier. 2000. Intraspecific variation in home range overlap with habitat quality: a comparison
among brown bear populations. Evolutionary Ecology 14:39–60.
Metcalfe, N.B., N.H.C. Fraser, and M.D. Burns. 1999. Food availability
and the nocturnal vs. diurnal foraging trade-off in juvenile salmon.
Journal of Animal Ecology 68:371–381.
Olsson, O., J.S. Brown, and H.G. Smith. 2002. Long- and short-term state
dependent foraging under predation risk: an indication of habitat
quality. Animal Behavior 63:981–989.
Orpwood, J.E., S.W. Griffiths, and J.D. Armstrong. 2006. Effects of food
availability on temporal activity patterns and growth of Atlantic
salmon. Journal of Animal Ecology 75:677–685.
Ortega, Y.K., K.S. McKelvey, and D.L. Six. 2006. Invasion of an exotic
forb impacts reproductive success and site fidelity of a migratory
songbird. Oecologia 149:340–351.
Ottonetti, L., L. Tucci, and G. Santini. 2006. Recolonization patterns of
ants in a rehabilitated lignite mine in central Italy: potential for the
use of Mediterranean ants as indicators of restoration processes.
Restoration Ecology 14:60–66.
Pejchar, L., K.D. Holl, and J.L. Lockwood. 2005. Hawaiian honeycreeper
home range size varies with habitat implications for native Acacia
koa forestry. Ecological Applications 15:1053–1061.
Persons, M.H., S.E. Walker, and A.L. Rypstra. 2002. Fitness costs and
benefits of antipredator behavior mediated by chemotactile cues in
the wolf spider Pardosa milvina (Araneae: Lycosidae). Behavioral
Ecology 13:386–392.
Persson, A., and M. Stenberg. 2006. Linking patch-use behavior, resource
density, and growth expectations in fish. Ecology 87:1953–1959.
Pidgeon, A.M., V.C. Radeloff, and N.E. Mathews. 2006. Contrasting
measures of fitness to classify habitat quality for the black-throated
sparrow (Amphispiza bilineata). Biological Conservation 132:
199–210.
Pomara, L.Y., R.J. Cooper, and L.J. Petit. 2003. Mixed-species flocking
and foraging behavior of four Neotropical warblers in Panamanian
shade coffee fields and forests. Auk 120:1000–1012.
Repasky, R. 1996. Using vigilance behavior to test whether predation promotes habitat partitioning. Ecology 77:1880–1887.
Ricketts, T.H. 2004. Tropical forest fragments enhance pollinator activity
in nearby coffee crops. Conservation Biology 18:1262–1271.
Robertson, B.A., and R.L.. Hutto. 2006. A framework for understanding
ecological traps and an evaluation of existing evidence. Ecology 87:
1075–1085.
Restoration Ecology
JUNE 2008
Animal Behavior and Restoration Success
Rouquette, J.R., and D.J. Thompson. 2007. Patterns of movement and
dispersal in an endangered damselfly and the consequences for its
management. Journal of Applied Ecology 44:692–701.
Ruiz-Jaen, M.C., and T.M. Aide. 2005. Restoration success: how is it
being measured? Restoration Ecology 13:569–577.
Sxekercioğlu, Cx. H. 2006. Increasing awareness of avian ecological function. Trends in Ecology and Evolution 21:464–471.
The Society for Ecological Restoration International Science and Policy
Working Group. 2004. The SER International Primer on Ecological
Restoration http://www.ser.org, Society for Ecological Restoration
International, Tucson, Arizona.
Shepherd, P.C.F., and J.S. Boates. 1999. Effects of a commercial baitworm harvest on semipalmated sandpipers and their prey in the Bay
of Fund Hermispheric Shorebird Reserve. Conservation Biology 13:
347–356.
Slabbekoorn, H., and M. Peet. 2003. Birds sing at a higher pitch in urban
noise: great tits hit the hight notes to ensure that their mating calls
are heard above the city’s din. Nature 424:267.
Stauss, M.J., J.F. Burkhardt, and J. Tomiuk. 2005. Foraging flight distances as a measure of parental effort in blue tits, Parus caeruleus,
differ with environmental conditions. Journal of Avian Biology 36:
47–56.
Summerville, K.S., A.C. Bonte, and L.C. Fox. 2007. Short-term temporal
effects on community structure of Lepidoptera in restored and remnant tallgrass prairies. Restoration Ecology 15:179–188.
Sun, J.W.C., and P.M. Narins. 2005. Anthropogenic sounds differentially
affect amphibian call rate. Biological Conservation 121:419–427.
Taillon, J., D.G. Sauvé, and S.D. Côté. 2006. The effects of decreasing
winter diet quality on foraging behavior and life-history traits of
white-tailed deer fawns. Journal of Wildlife Management 70:
1445–1454.
Tuberville, T.D., E.E. Clark, K.A. Buhlmann, and J.W. Gibbons. 2005.
Translocation as a conservation tool: site fidelity and movement of
repatriated gopher tortoises (Gopherus polyphemus). Animal Conservation 8:349–358.
Van Bael, S.A., and J.D. Brawn. 2005. The direct and indirect effects of
insectivory by birds in two contrasting Neotropical forests. Oecologia 145:658–668.
Vaughan, N., G. Jones, and S. Harris. 1996. Effects of sewage effluent on
the activity of bats (Chiroptera: Vespertilionidae) foraging along
rivers. Biological Conservation 78:337–343.
Vaughn, C.C., D.E. Spooner, and H.S. Galbraith. 2007. Context-dependent species identify effects within a functional group of filter-feeding
bivalves. Ecology 88:1654–1662.
JUNE 2008
Restoration Ecology
Vos, M., and L. Hemerik. 2003. Linking foraging behavior to lifetime
reproductive success for an insect parasitoid: adaptation to host distributions. Behavioral Ecology 14:236–245.
Walters, J.R., S.J. Daniels, J.H. Carter, and P.D. Doerr. 2002. Defining
quality of red-cockaded woodpecker foraging habitat based on habitat use and fitness. Journal of Wildlife Management 66:1064–1082.
Watson, M., N.J. Aebischer, and W. Cresswell. 2007. Vigilance and fitness
in grey partridges Perdix perdix: the effects of group size and foraging-vigilance trade-offs on predation mortality. Journal of Animal
Ecology 76:211–221.
Wauters, L.A., S. Bertolino, M. Adamo, S. Van Donegan, and G. Tosi.
2005. Food shortage disrupts social organization: the case of red
squirrels in conifer forests. Evolutionary Ecology 19:375–404.
Wellenreuther, M., and S.D. Connell. 2002. Responses of predators to prey
abundance: separating the effects of prey density and patch size.
Journal of Experimental Marine Biology and Ecology 273:61–71.
Wenny, D.G., and D.J. Levey. 1998. Directed seed dispersal by bellbirds
in a tropical cloud forest. Proceedings of the National Academy of
Sciences of the United States of America 95:6204–6207.
West, K.A. 2000. The Lake Ontario migratory songbird study: a case
study of the challenges and rewards of using volunteers in ornithological research. Pages 236–238 in R. Bonney, D.N. Pashley, R.J.
Cooper, and L. Niles, editors. Strategies for bird conservation: the
partners in flight planning process, Proceedings of the 3rd Partners
in Flight Workshop. Cape May, New Jersey, 1–5 October 1995. Proceedings RMRS-P-16. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Ogden, Utah.
Weston, M., M.. Fendley, R. Jewell, M. Satchell, and C. Tzaros. 2003. Volunteers in bird conservation: insights from the Australian threatened
bird network. Ecological Management and Restoration 4:205–211.
Winker, K., J.H. Rappole, and M.A. Ramos. 1995. The use of movement
data as an assay of habitat quality. Oecologia 101:211–216.
Wunderle, J.M. 1997. The role of animal seed dispersal in accelerating
native forest regeneration on degraded tropical lands. Forest Ecology and Management 99:223–235.
Yang, L.H. 2006. Periodical cicadas use light for oviposition site selection.
Proceedings of the Royal Society Biological Sciences Series B 273:
2993–3000.
Zahawi, R.A., and C.K.. Augspurger. 2006. Tropical forest restoration:
tree islands as recruitment foci in degraded lands of Honduras. Ecological Applications 16: 464–478.
Zerbe, S., and D. Kreyer. 2006. Introduction to special section on ‘‘Ecosystem restoration and biodiversity: how to assess and measure biological diversity’’? Restoration Ecology 14:103–104.
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