Boyle Effects of Nonconsumptive Recreation in Wildlife a Review

• Periodical List
• PLoS I
• PMC5145168

PLoS One. 2016; 11(12): e0167259.

Effects of Recreation on Animals Revealed every bit Widespread through a Global Systematic Review

Courtney L. Larson

^one Department of Fish, Wildlife, and Conservation Biological science, Colorado Country University, Fort Collins, Colorado, Usa of America

Sarah Eastward. Reed

¹ Section of Fish, Wild fauna, and Conservation Biology, Colorado State Academy, Fort Collins, Colorado, United states of America

² North America Program, Wildlife Conservation Order, Bozeman, Montana, United States of America

Adina Thou. Merenlender

³ Department of Environmental Science, Policy, and Direction, University of California-Berkeley, Berkeley, California, United states of America

Kevin R. Crooks

ⁱ Department of Fish, Wildlife, and Conservation Biology, Colorado State Academy, Fort Collins, Colorado, United states of America

Hideyuki Doi, Editor

Received 2015 Dec 1; Accepted 2016 Nov eleven.

Supplementary Materials

S1 Appendix: Articles near recreation effects on animals included in the literature review. (DOCX)

GUID: 9F11F669-B18D-4E6E-9321-E5933FC62D03

S1 File: Access database containing information extracted from reviewed papers. (ACCDB)

GUID: 429F342F-361E-43DC-A0BC-74E07807B606

S1 Table: PRISMA checklist. (DOC)

GUID: 2DCB5952-27D0-4FA2-8FFC-A6195FB9543B

Data Availability Statement

All relevant data are inside the newspaper and its Supporting Information files.

Abstruse

Outdoor recreation is typically causeless to be compatible with biodiversity conservation and is permitted in most protected areas worldwide. Nevertheless, increasing numbers of studies are discovering negative furnishings of recreation on animals. We conducted a systematic review of the scientific literature and analyzed 274 manufactures on the effects of non-consumptive recreation on animals, across all geographic areas, taxonomic groups, and recreation activities. Nosotros quantified trends in publication rates and outlets, identified knowledge gaps, and assessed evidence for furnishings of recreation. Although publication rates are low and knowledge gaps remain, the evidence was articulate with over 93% of reviewed articles documenting at least 1 upshot of recreation on animals, the majority of which (59%) were classified equally negative effects. Almost articles focused on mammals (42% of articles) or birds (37%), locations in North America (37.7%) or Europe (26.6%), and individual-level responses (49%). Meanwhile, studies of amphibians, reptiles, and fish, locations in Due south America, Asia, and Africa, and responses at the population and community levels are lacking. Although responses are likely to exist species-specific in many cases, some taxonomic groups (e.g., raptors, shorebirds, ungulates, and corals) had greater testify for an effect of recreation. Counter to public perception, non-motorized activities had more evidence for a negative effect of recreation than motorized activities, with effects observed one.2 times more frequently. Snow-based activities had more prove for an effect than other types of recreation, with effects observed one.3 times more frequently. Protecting biodiversity from potentially harmful effects of recreation is a primary business organisation for conservation planners and land managers who face increases in park visitation rates; accordingly, there is demand for science-based information to help solve these dilemmas.

Introduction

Visitation to protected areas, ranging in telescopic from international ecotourism to local park visits, was recently estimated at viii billion visits per year [1]. In the United States, the number of participants in outdoor recreation increased by 7.v% and full company days increased by 32.5% between 2000 and 2009 [two]. Driven in part by rapid growth in international tourism [iii], recreation and ecotourism are also expanding in the developing globe [4]; visits to protected areas in Africa, Asia, and Latin America increased by 2.v to 5% between 1992 and 2006 [5].

Recreation is commonly assumed to be uniform with biodiversity conservation, in contrast to more than well-known threats such equally population growth and evolution at protected expanse edges [vi,vii] or subsistence apply within reserves to help sustain local livelihoods [viii]. About protected areas accept a dual mandate to conserve biodiversity and improve homo welfare through resource use or outdoor recreation [eight,ix]. Accordingly, recreation is permitted in over 94% of International Union for Conservation of Nature (IUCN) protected areas globally (categories Ib-VI; [10,11]). In the United States and other developed nations, providing opportunities for outdoor recreation has historically been an important reason for the designation of protected areas [12], whereas in the developing world, ecotourism has been embraced as a potential win-win solution for poverty consolation and conservation [8]. Furthermore, at that place are numerous benefits of outdoor recreation for man health and communities. People with access to natural areas have lower bloodshed rates [13], and outdoor play promotes mental and physical health in children [fourteen]. Recreation and ecotourism tin can also exist a source of economic revenue for protected areas and the communities around them [fifteen,16], and can aid garner support for conservation [17].

Despite these benefits, in that location is growing recognition that outdoor recreation tin have negative impacts on biological communities. Recreation is a leading factor in endangerment of plant and creature species on United States federal lands [18], and is listed as a threat to 188 at-risk bird species globally [19]. Furnishings of recreation on animals include behavioral responses such as increased flight and vigilance [xx,21]; changes in spatial or temporal habitat apply [22,23]; declines in affluence, occupancy, or density [9,24,25]; physiological stress [26,27]; reduced reproductive success [28,29]; and altered species richness and customs composition [30,31]. Many species respond similarly to human disturbance and predation run a risk, pregnant that disturbance caused by recreation tin force a merchandise-off between risk avoidance and fettle-enhancing activities such equally foraging or caring for young [32].

Although there is a growing body of empirical studies of the effects of recreation on animals, a contempo global review of the scientific literature does not exist. Early reviews [33–36] provide valuable definitions and conceptual frameworks, but were non systematic and need updating to reflect studies published in recent decades. In addition, contemporary reviews have restricted their telescopic past location or habitat blazon [37–39], taxonomic grouping [40–45], or recreation activity [46–48].

We conducted a global review of the published scientific literature to synthesize effects of non-consumptive recreation across all animal taxa. Such a review adds to the evidence base necessary to assist bridge the gap between conservation science and practise [49]. To aid decision-makers faced with dilemmas about managing the need for recreation while trying to fulfill mandates to protect species, it is critical to understand the degree to which biodiversity conservation and recreation are uniform, and under what circumstances. Starting time, we examined trends in recreation research, including publication rates over time, geographic distribution, and study blueprint. Second, we investigated which taxonomic groups were most normally studied, and which had more or less bear witness for effects of recreation. Similarly, we investigated which recreation activities and types of responses (e.1000., behavioral, abundance, or survival) were most frequently measured, and what effects were observed. Finally, we examined management strategies proposed by the authors to avoid or mitigate these effects.

Methods

Search strategy

Because our objective was to locate studies of all animal species and all types of recreation, our search protocol was designed to produce a broad list of articles. Nosotros did non include taxonomic keywords since titles and abstracts ofttimes refer only to the written report'southward focal species. Instead, we limited the search to journals within iv categories within the Establish for Scientific Information Web of Scientific discipline database (Thompson Reuters, New York, NY, USA) that were the about relevant to our goals: biodiversity conservation, environmental, zoology, and behavioral sciences. From this list, we removed journals that were non published in English, or could not exist reasonably expected to publish articles on recreation and animals (n = 166 journals included in the final list). We so searched the database with the Boolean search string: (ts = (touris* OR recreat*) And then = (journal list)), where ts indicates topic keywords and so restricts the search to the list of 166 journals described above. This search strategy has high sensitivity (the proportion of all relevant information that the search locates) and depression specificity (the proportion of search results that are relevant), which helps reduce bias and increase repeatability [50]. To reduce the effect of dissemination bias in our analysis, nosotros included articles published in regional and bottom-known journals as well as the most widely-read publications [51]. Since our search strategy fabricated employ of the periodical category feature within Web of Science, nosotros were not able to replicate the search in other databases. However, our strategy produced a more thorough and comprehensive list of articles than if we had restricted our search with taxonomic keywords.

Screening and data extraction

Our keyword search (performed 30 January 2013 and once more on 21 March 2016) resulted in a comprehensive listing of 2,306 articles. We first reviewed titles and abstracts and eliminated plain irrelevant records (due east.chiliad., tourism management papers with no wildlife component; Fig i). We then reviewed the total text of the remaining 403 articles and assessed them confronting our inclusion criteria, recording the reason for rejection if necessary [50]. Nosotros excluded consumptive activities, which we ascertain following Duffus and Dearden [34] equally activities that "purposefully remove or permanently bear on wildlife" (east.g., hunting, line-fishing). We focused on non-consumptive forms of recreation (e.chiliad., hiking, skiing) because these activities are permitted more widely throughout protected areas. However, studies examining consumptive activities as a source of disturbance for not-target species (eastward.g., effects of angling on waterbirds; [52]) were retained. Nosotros also rejected articles if they did not study one or more animal species (due north = 2), did not test effects of non-consumptive recreation via a statistical test (n = 70), did not collect empirical field data (e.g., were review or simulation manufactures; n = 23), studied the effects of recreation infrastructure independently of human being action (e.yard., presence of ski lifts; north = 20), or examined recreation as a vector for invasive species dispersal (n = 14). Experimental treatments designed to mimic recreational activities were included. The final list included 274 articles (S1 Appendix) with 2,048 singled-out results.

PRISMA literature search flow diagram.

The number of studies that were located, retained, and discarded are shown at each phase of the literature review process.

Data collected from each article included publication information, geographic location (state and continent), study design, taxonomic grouping(s), recreation activities, response types and effects institute, and management recommendations (Tabular array 1). For articles that studied multiple species, recreation activities, or response types, we treated each combination of variables as a separate "effect," rather than attempting to determine an overall effect for each article, which would ignore valuable findings from inside each article. For example, Banks and Bryant [24] examined the furnishings of hiking and dog-walking on bird affluence and richness, so we recorded four combinations of "results" in our database. While results from the aforementioned study frequently rely on the same animal populations, locations, and data drove efforts, we examined each result separately since effects often differed. Because each commodity could be considered an experimental unit, we added a random effect for article in the analysis to control for this potentially misreckoning factor (see "Statistical analysis").

Table ane

List of variables collected from articles included in the review of the effects of non-consumptive recreation on animals.

Category	Variable	Description or list of categories	Data type
Publication	Author(due south)		text
	Title		text
	Journal		text
	Journal type	Beliefs, conservation, ecology, ecosystem/region-specific, general biology, taxa-specific, zoology/wildlife, other	categorical
	Publication twelvemonth		numeric
Geographic	Continent		categorical
	Country		text
	Habitat type	Agronomical, beach, desert, forest, freshwater, grassland, marine, polar, shoreline, urban, scrub/shrub, tundra, wetland, other	categorical
Study design	Measure out of recreation*	Direct ascertainment, experimental handling, expert stance, remote monitoring, permitted use, proxy	categorical
	Experiment	Was information technology an experimental report?	yes/no
	Control	Did the study include a control handling? (eastward.m. a "no-recreation" site)	yes/no
	Replication	Did the written report replicate treatments, written report sites, observation periods, etc?	yeah/no
Event	Result*	Did the authors discover a significant recreation impact?	yes/no
	Upshot direction*	Positive, negative, unclear	categorical
Taxonomic	Multiple species	Were multiple species studied?	aye/no
	Taxa grouping	Amphibian, bird, fish, invertebrate, mammal, reptile	chiselled
	Scientific name*		text
	Common proper name*		text
Recreation	Activity*	Tall skiing, beach utilise, biking, boating (non-motorized), camping ground, nordic ski/snowshoeing, dog-walking, equestrian, hiking/running, motorized (boat), motorized (country), motorized (snow), swimming/diving, wildlife feeding, wildlife viewing (boat), wildlife viewing (state), other (aquatic), other (terrestrial)	categorical
Response	Type*	Abundance, behavioral, customs (species richness, diversity, or limerick), occurrence, physiological, reproductive, survival, other	categorical
Management	Recommendations	Cap visitation, amend infrastructure, rule change, staff training, spatial restrictions, temporal restrictions, visitor instruction, none, other	chiselled

The "effect" variable (Tabular array 1), which was the response variable for several of our research questions, was a binary variable indicating whether the recreation effect documented by the authors was statistically pregnant (as defined past the authors). We categorized all pregnant furnishings as negative, positive, or unclear. Negative responses were consistent with the following effects of recreational disturbance at the community, population, or individual (behavioral or physiological) levels: decreased species richness or variety; decreased survival, reproduction, occurrence, or affluence; behaviors typically causeless to reflect negative responses to anthropogenic disturbance (due east.yard., decreased foraging or increased vigilance); and physiological condition typically causeless to reflect disturbance effects (e.g., decreased weight or increased stress). Conversely, positive responses were in the contrary direction. Nosotros were unable to classify some responses equally positive or negative and labeled them "unclear." Examples of unclear effects were behavioral responses that did non have obvious fettle consequences (due east.thousand., decreased vocalizing) and results with non-linear responses (e.g., highest reproductive success at an intermediate level of recreation). Nosotros notation that positive responses do not necessarily imply beneficial outcomes for biodiversity conservation; for example, an increase in species richness could be attributable to an increase in non-native species.

We circumspection that a statistically significant upshot of recreation does not necessarily provide insight into the outcome'southward magnitude or biological significance. Authors may also include statistically significant results while omitting not-pregnant findings due to publication bias [53]. A formal meta-analysis framework can help researchers summarize event sizes and detect and adjust for publication bias [54], only the study pattern must be similar beyond all studies included, with comparable predictor and response variables [55]. This was not feasible given the broad scope of our review, and accordingly, we do not make statistical comparisons amid groups. Ultimately, we believe our approach provides a meaningful representation of the weight of evidence that currently exists.

Publication trends and geographic distribution

We summarized the number of articles by publication yr, journal type, country, continent, and habitat blazon. Journals were classified into viii broad types using the journal title and online aims and scope statement to identify the appropriate master category. Articles were likewise assigned to one or more habitat classes on the basis of authors' descriptions (Table 1).

Study design

To examine how recreation studies accept been designed and conducted, we recorded the proportion of articles that used an experimental design and included controls and replication. For our purposes, whatsoever kind of an experimental treatment (e.g., experimental gunkhole passes almost a raptor nest; [56]) counted as an experimental design, and any treatment or site without recreation counted equally a control. We also examined the method used to measure recreation: straight ascertainment (with man observers), experimental treatment (e.thousand., researchers simulating recreation activities), practiced opinion, remote monitoring (e.1000., automatic counters), permitted use (e.g., whether a site was open to a specific recreational activity), or proxy variables (eastward.g., motorcar counts).

Taxonomic groups

We examined differences in research focus and prove for recreation effects amidst half dozen broad taxonomic groups: amphibians, birds, fish, invertebrates, mammals, and reptiles. Nosotros divided groups with sufficient sample size (≥ fifteen results on ≥ three different species) into narrower taxonomic classifications (Classes for invertebrates and fish; Orders for birds, mammals, and reptiles; amphibians were omitted due to pocket-size sample size). Nosotros and then subdivided Classes or Orders with sufficient sample sizes (≥ 15 results on ≥ 3 different species) one time once more into Orders or Families. We also grouped species by their IUCN status [57].

Recreation activities

Nosotros grouped recreation activities into eighteen types (Table 1) and created broader categories for more than general comparisons: winter terrestrial (snowfall and ice-based activities such equally skiing and snowmobiling), summer terrestrial (land activities not requiring snow or ice), and aquatic activities. We as well compared motorized and non-motorized activities.

Response types

We categorized animal responses into viii types: community (species richness, diverseness, or limerick metrics), survival, reproduction, abundance, occurrence, behavior, and physiological measures, as well as "other" responses (due east.g., sex ratio). For more full general comparisons, we also grouped the response types hierarchically into community-, population- (survival, reproduction, abundance, and occurrence), and private-level (beliefs and physiological) responses.

Management recommendations

To qualify the direction recommendations noted in the articles and provide a useful synthesis for state managers, we categorized recommended management actions every bit follows: spatial restrictions, capping visitation, increasing visitor educational activity, temporal restrictions, improving infrastructure, adding or changing rules, enforcement of existing rules, staff training, or "other" (Tabular array 2). Calls for additional inquiry, although common in the literature, were not considered to be management recommendations.

Table 2

General management recommendations suggested by authors of manufactures included in the review.

Recommendation	Examples	Frequency (%)*
Spatial restrictions	Designate a trail-free surface area inside protected surface area; establish minimum approach distances to animals	32.1
Visitor instruction	Brainwash SCUBA divers about the impacts of human contact on coral; instruct visitors nearly effects of noise on sensitive species	fifteen.0
Cap visitation	Limit the number of visitors that can enter the area per twenty-four hour period	14.ii
Temporal restrictions	Limit recreational access during the breeding season	13.one
Rule change	Restrict boat speed in sensitive areas; prohibit wild animals feeding	nine.9
Physical improvements	Restore habitat; install fencing around sensitive areas	9.v
Other	Species translocations; increased use of private land for conservation	8.eight
Enforcement	Enforce leash laws; go along people on trails	6.9
Staff grooming	Train staff to recognize signs of animal disturbance	2.two
No recommendations		40.five

Statistical analysis

We used linear regression to assess trends in the total number of articles over time besides as the proportion of included articles out of the total publication volume in the selected journals. To assess gaps in the literature, we used chi-square goodness of fit tests to determine if the distribution of articles differed significantly from an expected distribution. For periodical type, the expected distribution was the proportion of journals in the periodical set that belonged to each blazon. For geographic distribution, we compared the distribution of manufactures by continent to the total country area and man population density of each continent. For IUCN status and taxonomic groups, the expected distribution was the number of known species in each grouping, starting with the broadest groups and progressing down to Family when possible [57]. Nosotros did not use chi-square tests if articles were counted nether more than i category (e.g., articles examining multiple types of recreation, such as hiking, biking, and equestrian) since this violates the assumption of independence.

We estimated the corporeality of evidence for a recreation impact equally the overall pct of results that establish a statistically pregnant upshot of recreation. These percentages were estimated for results summarized by taxonomic groups, recreation activities, and response types. Considering nigh manufactures included multiple results, the percentages (± SE) we report are least-squares means and standard errors obtained from models that included article equally a random effect. We used generalized linear mixed models (GLMMs) with a logit link part to estimate the frequency of overall effects among taxonomic groups, recreation activities, and response types, and we used proportional odds models [58] to estimate the proportion of overall effects that were negative, positive, or unclear. All statistical analyses were conducted in R using packages lme4, ordinal, and lsmeans [59–62].

Results

Publication trends and geographic distribution

The earliest articles discovered by our search were published in 1981, and the peak year was 2008 with 23 articles. The number of manufactures published per year that met our criteria increased 23.5% on average per twelvemonth from 1981 to 2015 (β = 0.66, 95% CI = (0.53, 0.lxxx), p < 0.0001). This increase was non solely a result of increasing publication volume; the proportion of included articles out of the total articles published in the journal set increased by 8.eight% on average per twelvemonth (β = 0.000043, 95% CI = (0.000033, 0.000053), p < 0.0001; Fig ii). The distributions of the journal set into journal types (e.m., conservation, wild fauna) and private articles into journal types were significantly different (χⁱⁱ = 632.4, df = vii, p < 0.0001). Most of the included articles were published in conservation (38.7%) and wild animals (nineteen.vii%) journals, followed by ecology (13.v%), taxa-specific (13.1%), ecosystem or region-specific (nine.9%), and beliefs journals (3.three%); very few manufactures were published in full general biology (0.seven%) or other (0.7%) journal categories.

Published articles on the effects of non-consumptive recreation on animals by publication year.

The numbers of manufactures are shown as raw numbers (shaded bars) and as percentages of the overall publication book in the periodical set used in this review (trendline; a 2nd order polynomial part).

Geographically, studies of recreation on animals were conducted by and large in Northward America (37.7%), Europe (26.6%), and Oceania (13.1%), and relatively few in S America (9.1%), Asia (5.v%), Africa (5.one%), and Antarctica (2.9%; Fig 3A). This distribution among continents was not proportional to the land area (χⁱⁱ = 366.three, df = 6, p < 0.0001) nor human population density (χ² > 500, df = vi, p < 0.0001) of the continents. The United States deemed for 27.0% of the articles, followed by Australia (seven.7%), Spain (v.8%), New Zealand (5.v%), the United Kingdom (iv.seven%), Argentina (4.4%), and Canada (4.four%). About studies were conducted in forest (35.iv%), marine (23.4%), grassland (15.7%), and shoreline (13.nine%) habitats (Fig 3B). The least well-studied habitat types were polar (ii.ix%), and desert (one.v%), also as human-modified habitats (agricultural and urban, representing 10.two% of articles combined).

Distribution of published articles on the effects of non-consumptive recreation on animate being species.

Panel (a) shows the countries where studies were conducted, and panel b) shows the distribution of studies into major habitat type(s). Since some studies involved multiple habitat types, the sum (424) is greater than the total number of articles (274). Numbers at the end of confined correspond the total number of articles in each category.

Study design

Less than one-tertiary (thirty.iii%) of the articles contained an experimental component, and 60.9% of articles independent controls. Almost (85.iv%) articles had replication of study sites, treatments, or groups. Straight observation was the most common method for measuring recreation (38.1% of results), followed by proxy variables (19.9%), skillful opinion (19.6%), and experimental treatment (18.0%). Permitted use equally a mensurate of recreation was less common (12.5%), equally was remote monitoring (six.7%).

Taxonomic groups

Enquiry endeavor in our sample of manufactures was non proportional to the number of species within all taxonomic groups at the broadest level (χ² = 377.three, df = 5, p < 0.0001), nor to the number of species in bird (χ² = 988.7, df = five, p < 0.0001) and mammal (χ² = 290.3, df = 3, p < 0.0001) Orders or invertebrate Classes (χ² = 98.1, df = 2, p < 0.0001; Fig four). Mammals (41.6%) and birds (36.9% of articles) were the focus of the majority of recreation studies, followed by invertebrates (12.4%), reptiles (v.5%), fish (five.i%), and amphibians (0.7%). Studies of a single species were more common (69.0%) than those that examined at to the lowest degree two species. Research on mammals focused mainly on ungulates (28.9%), carnivores (26.iii% of manufactures), cetaceans (21.9%), and primates (12.three%). Among birds, the nigh normally researched Orders were Passeriformes (passerine birds; 24.viii% of articles), Charadriiformes (wading birds and gulls; 23.eight%), Sphenisciformes (penguins; 13.9%), and Accipitriformes (hawks, eagles, vultures; ix.9%). Many of the invertebrate studies (35.2%) focused on the effects of snorkeling or SCUBA diving on corals, followed by studies on arachnids, bivalves, and insects (each 14.7%). The about commonly studied fish Course was Actinopterygii (ray-finned fish; 57.1%), followed past Chondrichthyes (sharks, stingrays; 42.9%). Research on reptiles focused on Orders Squamata (lizards, snakes; 78.6%) and Testudines (turtles; 21.four%).

Bear witness for an effect of recreation past taxonomic group.

Evidence is measured equally the proportion of results that were statistically significant. For articles that studied multiple recreation activities, species, or response variables, each combination of variables was treated every bit a separate result. Common names are examples of species occurring in the included articles. We present taxonomic groups that have at least 15 results and 5 species represented; the remaining taxa are included in "other" categories for comparative purposes. Numbers post-obit confined show the number of results, number of articles, and count of unique species. Articles that studied functional groups or communities rather than individual species (e.g., insectivorous birds) were added to the relevant "other" category and were not counted as species. Error bars show standard error for the sum of all effects.

We identified the IUCN status of the species for 68.7% of results, representing 305 unique species; the remaining results examined multiple species or species not evaluated by the IUCN. The distribution of these results into IUCN status categories was not proportional to the distribution of all animal species into these categories (χ² = 108.3, df = 5, p < 0.0001), with many more species than expected in the least concern category (80.7%), slightly more than than expected in the near threatened (6.9%), and fewer than expected in the data deficient (1.half-dozen%), vulnerable (6.5%), endangered (three.half dozen%), and critically endangered (0.1%) categories. Endangered species that were studied included three mammals (blackness howler monkey Alouatta pigra, Hector's dolphin Cephalorhynchus hectori, and the Barbary macaque Macaca sylvanus), three fish (dusky grouper Epinephelus marginatus, Nassau grouper Epinephelus striatus, and the brownstriped gaunt Anisotremus moricandi), two birds (Egyptian vulture Neophron percnopterus and the xanthous-eyed penguin Megatypes antipodes), two reptiles (wood turtle Glyptemys insculpta and Lilford's wall cadger Podarcis lilfordi), and the boulder star coral Montastraea annularis. The simply critically endangered animals were the Western lowland gorilla Gorilla gorilla gorilla and the Mexican howler monkey Alouatta palliata mexicana.

Of the 274 articles analyzed, 93.1% documented at least i effect of recreation on animal populations, individuals, or communities. Negative effects of recreation were the nigh frequent (59.4%), followed by unclear (25.9%) and positive (xiv.seven%) furnishings. Most (83.half-dozen%) of the unclear effects were behavioral responses.

Taxonomic groups with the most negative furnishings were amphibians (68.4 ± 20.two% of results), reptiles (56.3 ± 9.two%), and invertebrates (51.0 ± 5.1%), while mammals (5.iii ± 1.9%) and birds (4.3 ± two.0%) had the most positive effects (Fig iv). Among bird Orders, evidence for overall and negative effects was greatest in Accipitriformes (e.g., eagles, hawks; 70.7 ± 10.seven and 47.seven ± 24.4%; Fig 4). Positive furnishings were greatest in Anseriformes (east.g., ducks, swans; 10.4 ± 22.6%) and Passeriformes (passerine birds; six.nine ± vii.7%). Evidence of negative effects among Charadriiformes Families was greatest in Charadriidae (e.g., plovers, lapwings; 58.2 ± xviii.vi%). Among Passeriformes Families, Corvidae (e.g., crows, choughs) had the most positive furnishings (56.0 ± 4.ix%). Amidst mammal Orders, Artiodactyla (even-toed ungulates) had the about negative furnishings (48.5 ± 8.0%) and Rodentia (rodents) had the near positive effects (14.4 ± 12.3%). At the family level, Bovidae (e.g., bison, bighorn sheep) had past far the most overall effects (93.8 ± xix.iii%) and Delphinidae (dolphins) was besides high (70.eight ± 6.viii%). Several invertebrate Classes had considerable negative effects, including Anthozoa (corals; 56.vi ± four.ii%), Gastropoda (east.g., snails, slugs; 55.5 ± 6.7%), and "other" (e.chiliad., insects, crabs; 51.4% ± half dozen.0%). Finally, the "other" grouping of fish Classes (e.1000., sharks, stingrays) had more testify for an overall and positive effect (64.9 ± viii.seven% overall and 25.viii ± fifteen.7% positive) than Actinopterygii (ray-finned fish; 34.viii ± viii.5% overall and 5.4 ± 9.two% positive). Of the reptile orders, Club Testudines (turtles) had more overall effects (75.0 ± 12.five%) effects than Order Squamata (lizards, iguanas; 52.3 ± vii.5). For both Orders, all of the effects were negative. Depression sample sizes precluded comparisons among amphibian taxa.

Recreation activities

The articles in our sample examined a broad variety of recreation activities (Fig 5A). Summer terrestrial activities were the nigh common, studied by 66.7% of manufactures, followed by aquatic (27.8%) and winter terrestrial (5.6%). Motorized forms of recreation, including off-highway vehicles, snowmobiles, and motorized boats, were examined in 26.3% of articles. Hiking was studied much more often than whatsoever other recreation action (27.5% of articles). Wild fauna viewing was also relatively frequently studied, with x.three% of articles studying land-based and 6.6% studying boat-based wildlife viewing.

Recreation activities in the manufactures included in this review.

Panel (a) shows the percent of manufactures that included each recreation activity (numbers of articles follow the confined), and panel (b) shows the percent of results in which a statistically meaning effect of recreation on an creature species was observed (number of results follow the bars). Total percentages are divided into negative, positive, and unclear effects of recreation. Error bars testify standard error for the sum of all furnishings.

Wintertime terrestrial activities had the most evidence of overall (77.3 ± 7.8% of results; Fig 5B) and negative (64.4 ± 10.1%) effects, compared to 58.5 ± 2.seven% (overall) and 39.vi ± 4.half-dozen% (negative) for other terrestrial and 57.0 ± 3.8% (overall) and 33.iv ± 7.1% (negative) for aquatic activities. Although motorized and not-motorized activities had similar evidence for overall furnishings (57.0 ± 5.ane% and 58.iv ± ii.5%), non-motorized had greater negative effects (twoscore.iii ± four.0% versus 34.0 ± 8.vi%). Activities with the most show of overall effects included each of the snowfall activities (cross-country ski/snowshoeing: 81.0 ± 8.6%, motorized–snow: 77.8 ± 13.9%, alpine skiing: 71.0 ± 8.2%), as well as boat-based wild animals viewing (65.4 ± 5.4%) and beach use (64.8 ± viii.ii%; Fig 5B).

Response types

Response types were not studied evenly; behavioral (45.5% of articles) and abundance (24.1%) responses to recreation were the nigh mutual (Fig 6A). Only ix.3% of articles measured community metrics (species richness, diversity, or composition) and 1.nine% measured survival. Omitting survival responses due to small sample size, community responses had the most overall effects (64.half dozen ± half dozen.six% of results), followed by behavioral (63.5 ± 2.8%) and physiological (62.5 ± iv.9%) responses; reproductive responses (36.vii ± 6.3%) had the fewest overall effects (Fig 6B). Physiological (52.7 ± 4.viii%) and occurrence (51.iii ± 4.6%) responses had the most negative furnishings, while behavioral responses had the well-nigh positive effects (9.8 ± 2.5%).

Types of fauna responses to recreation in the articles included in this review.

Response types take been categorized into community-, population-, and individual-level responses. Panel a) shows the percent of articles in which each response type is tested (numbers of articles follow the confined). Panel b) shows the percent of results in which a statistically significant effect of recreation on an animal species was observed (number of results follow the bars). Total percentages are divided into negative, positive, and unclear effects of recreation. Error bars show standard error for the sum of all effects.

Management recommendations

More than than i-third (forty.5%) of the included manufactures did not provide direction recommendations (Tabular array 2). Of those that did include recommendations, the most common types were spatial restrictions (32.1%), visitor education (15.0%), and limiting visitation (xiv.2%), Enforcement of existing rules (half dozen.9%) and staff training (2.2%) were the to the lowest degree oft suggested direction categories.

Discussion

Although published research on recreation effects on animals increased past an society of magnitude from 1981 to 2015, the percentage of the literature devoted to the subject remains small (0.16% of publication volume of the target journals in the peak yr), and many gaps in cognition remain. The literature is geographically biased in favor of North America and Europe, and taxonomically biased toward birds and mammals. Over 93% of reviewed articles documented at to the lowest degree one effect of recreation, and as expected, the bulk of these effects were negative. Not-motorized and wintertime terrestrial activities had notable testify for negative furnishings. Additionally, some of the to the lowest degree studied taxonomic groups (reptiles, amphibians, and invertebrates) had the greatest evidence for negative effects of recreation.

Though the amount of literature on this topic has increased in contempo decades, it may not be reaching a broad audience even among conservation scientists and wildlife ecologists. Over twenty% of manufactures were published in journals specific to a taxonomic group, geographic region, or ecosystem, whereas few were published in the broadest journals. Since the broadest journals are also among the highest-impact publications (due east.yard., Science, Nature), this could also indicate that the topic of recreation impacts on animals is non viewed every bit important inside the peer-reviewed literature.

The articles had a strong geographic bias toward North America and Europe. This reflects global patterns in visitation to protected areas since over lxxx% of visits occur in these two continents [i]. A surprising number of studies were conducted in Antarctica, as a issue of a growing ecotourism manufacture that frequently includes visits to penguin colonies [63]. Every bit South America, Africa, and Asia contain virtually of the earth'south biodiversity hotspots [64] as well equally popular ecotourism destinations including Brazil, S Africa, Thailand, and Indonesia [65], we encounter an immediate need for studies of recreation furnishings in these areas. The few studies conducted in tundra, polar, and desert habitat types is likely a event of low rates of recreation and tourism occurring in these areas. However, our findings and those of Sato et al. [39] about the impacts of alpine activities bespeak that it is an important area for future study.

Farther, the distribution of manufactures among wide taxonomic groups was skewed in favor of mammals and birds, a trend consistent with conservation science as a whole [66]. However, these are large, various groups that still warrant more research; for example, passerine birds were the most ofttimes studied avian Society in our prepare of articles, simply the 73 species examined therein comprise ~1% of the five,000+ species in the Order. In that location is too an urgent demand to understand more nigh the potential effects of recreation on invertebrates, fish, reptiles, and amphibians. We found but two articles on amphibians, but their known sensitivity to human disturbance [67] highlights the need to understand whether and how recreation affects them. Current inquiry on recreation effects on animals does not include many species of urgent conservation concern; only virtually 10% of species studied are globally threatened (IUCN status of critically endangered, endangered, or vulnerable). Recreation may not exist the primary reason for their endangerment, but it is a threat worth understanding because the disturbance may take place in the very protected areas designated to conserve these species. Finally, relatively few manufactures (31.0%) examined more 1 species, and studies of species from multiple trophic levels were especially rare (3.6%). More inquiry is needed on community-level effects of recreation, including potential cascading effects [68].

Examination of the report designs of the included articles revealed some notable trends. A fairly loftier percentage (30%) of articles included an experimental component; most of these were recreation treatments applied in lodge to compare behavioral responses. Over fourscore% of results examined recreation as a categorical variable, typically with three or fewer levels (e.g., low vs. high recreation activity). Though a categorical arroyo is simpler to implement and clarify, it limits the ability of researchers to evaluate how responses may change with different recreation intensities. It has proven difficult to develop hypothesized response curves representing how animals respond to increasing levels of recreational use due to the diversity of responses [69]. Future research should measure out recreation across intensity gradients to aid verify the existence of thresholds and the shape of these relationships.

Nearly (59%) of the effects of recreation on animals documented in the reviewed articles were negative effects. This was particularly true for reptiles, amphibians, and invertebrates, although sample sizes were low. Among invertebrate Classes, Anthozoa (corals) often had physical damage or reduced affluence in areas frequented by recreational defined [70,71]. Though the rate of negative furnishings was generally lower for birds, mammals, and fish, some lower taxonomic groups had more than show for negative effects of recreation. For example, Lodge Accipitriformes (e.g., eagles, hawks) had more evidence for negative effects compared to other bird Orders, consequent with a prior meta-analysis of human disturbance on nesting birds of prey [41]. Family Charadriidae (e.yard., plovers, lapwings) also had considerable evidence for negative effects of recreation, which parallels a recent study that establish that species from this Order (Charadriiformes) were more oft threatened by tourism than other bird Orders [19]. Of the mammals, Society Artiodactyla (eastward.thou., deer, bison) had substantial show for negative furnishings, mostly consisting of behavioral responses to recreation activity. Many researchers have investigated factors that influence ungulate flying responses, including speed of arroyo, animal and human group size, and habitat type [43,45]. For fish, several studies found negative physiological effects of wild fauna viewing on Grade Chondrichthyes (e.g., sharks, stingrays; [72,73]), and negative effects of diving on fish communities [70].

Evidence for positive effects of recreational activeness was much less common. Birds, particularly corvids, had more than bear witness for positive effects compared to most other broad taxonomic groups. Many corvids are urban adaptors [74], and several studies found that they apace habituate to human disturbance, allowing them to tolerate or even thrive in the presence of recreationists [75,76], sometimes at the expense of other species [77]. Mammals also had a relatively high rate of positive effects. Of the mammal Orders, rodents had the nearly evidence for positive effects; all only one of these effects were behavioral and near resulted from habituation (east.g., reduced flight responses in areas with higher levels of recreation; [78,79]. Habituation to recreation was discussed in many (39.4%) of the included articles and typically resulted in positive responses in our coding organisation (due east.m., reduced flight initiation distances in habituated animals), but whether habituation is a beneficial issue for animals (east.g., past reducing plush behavioral responses to humans) is unclear and warrants further study [80,81].

We found that non-motorized activities had more evidence for negative furnishings than motorized activities. Motorized activities are often expected to be more harmful to animals because of vehicle speed and racket [43], but our results suggest the opposite beyond a wide range of report locations and taxa. A few articles directly compared motorized and non-motorized activities; four mammals (guanaco Lama guanicoe, wolverine Gulo gulo, coyote Canis latrans, and bobcat Lynx rufus) showed behavioral or occurrence responses to not-motorized but non to motorized recreation [22,82,83], whereas the reverse was establish for Hector'southward dolphin (Cephalorhynchus hectori) behavior [84] and ghost crab (Ocypode quadrata) abundance [85]. Even so, motorized activities often cover larger spatial extents than non-motorized activities, and since most studies did not compare effects beyond multiple spatial scales, information technology is possible that their affect has been underestimated. Additionally, motorized vehicles can likewise crusade other types of harm not explored here, such equally soil loss and vegetation disturbance [86]. A meta-analysis designed to explicitly compare the magnitude of effects of motorized and not-motorized recreation would be a valuable contribution to the literature.

Our results too propose that winter terrestrial activities take greater evidence for effects on animals than summertime terrestrial or aquatic activities, though the number of articles was small. A recent review of winter recreation effects on animals [39] supports this conclusion, finding that over half of the reviewed articles reported overall detrimental furnishings, peculiarly on birds and on species richness and diverseness. There are several possible explanations for this upshot. Movement abroad from recreationists may exist more energetically plush in snowy conditions [87]. For many species, food availability and quality is lower during winter [82,88], limiting their ability to relocate to avert areas with human activity. At that place could too be habitat effects since vegetation in alpine and sub-alpine environments regenerates slowly, so habitat degradation caused by winter recreation could be more astringent than that caused by other recreational activities in more temperate climates [39,89].

Overall, authors observed individual-level (behavioral and physiological) and community-level effects more often than nearly population-level (occurrence, abundance, and reproduction) effects. Though rarely measured, negative effects of recreation on survival–a particularly important response to empathise for conservation purposes–were observed one.iv times more oft than the next highest response types (physiology and occurrence). Behavioral metrics, which were studied far more than oftentimes than other types of responses, may be popular considering they tin exist simpler to measure and accept been proposed equally a proxy for demographic parameters [90]. Nonetheless, behavioral metrics may not reflect the true population consequences of anthropogenic disturbance [91]. Study duration tin likewise influence conclusions; one long-term study establish that depression-level recreation had an effect on dolphin habitat use that was not observed in a short-term behavioral study [81,92], while some other found that brusque-term behavioral responses did not outcome in changes in the distribution or relative affluence of waterbirds [93].

Though nearly manufactures documented recreation effects, few presented specific, practical steps to minimize impacts. Most xl% of the manufactures did not describe whatsoever management or mitigation deportment, and many more contained only vague suggestions. We see a strong demand for empirical tests of the effectiveness of direction actions, which were rare. Encouraging examples of successful mitigation deportment do be, such every bit educating defined about fugitive damage to coral reefs [94], using volunteers to deter harassment of fur seals [95], and installing fences to plant disturbance-gratis areas [96,97]. This type of practical evaluation of direction strategies is disquisitional in assessing the ability of protected areas to meet demands for both recreational opportunities and the conservation of biodiversity. Interviewing practitioners would be a useful direction for time to come enquiry in order to assess the type and extent of management strategies currently being employed. Fifty-fifty where direction recommendations are provided in the scientific literature, information technology is unclear to what extent they are received by protected area managers [98]; a search of unpublished reports and other communications on the subject would help inform how well conservation scientists are reaching conclusion-makers.

The effects of recreation on animals is withal a relatively unknown and low-profile topic in the conservation science literature, despite growing evidence that detrimental impacts can occur from a broad variety of recreational activities. Farther, biophysical disturbances associated with recreation and tourism–including habitat conversion for roads and resorts, pollution from vehicles, and the spread of invasive species–are likely to have boosted furnishings [19], increasing the overall impact of the recreation and tourism industry. Recreation effects may also human action synergistically with other threats to biodiversity such as urbanization and land-use change [18], which may result in increased access for recreation. This is a troubling problem for managers and conservation practitioners, since recreation is an integral part of protected areas worldwide [12]. Finding an appropriate balance betwixt biodiversity conservation and outdoor recreation is complicated, especially since impacts vary among species and recreation activities. We must start by simply acknowledging that these uses are not necessarily compatible for all species, in all locations. This will make it easier to justify additional research on this topic, constitute restrictions on recreation, and encourage changes in the behavior of recreationists, leading to improved conservation outcomes.

Supporting Information

S1 Appendix

Articles almost recreation effects on animals included in the literature review.

(DOCX)

S1 File

Access database containing information extracted from reviewed papers.

(ACCDB)

S1 Table

PRISMA checklist.

(DOC)

Acknowledgments

We thank A. Hess and P. Turk of the Colorado State University StatLab for helpful statistical advice. Comments from R. Knight, C. Carroll, and South. Bombaci improved the manuscript.

Funding Statement

This report was funded by the California Department of Fish and Game (Local Assist Grant P1182112). The funders had no role in study pattern, data collection and analysis, decision to publish, or grooming of the manuscript.

Information Availability

All relevant data are within the paper and its Supporting Information files.

References

one. Balmford A, Light-green JMH, Anderson Thousand, Beresford J, Huang C, Naidoo R, et al. Walk on the Wild Side: Estimating the Global Magnitude of Visits to Protected Areas. PLOS Biol. 2015;13: e1002074 10.1371/journal.pbio.1002074 [PMC gratuitous commodity] [PubMed] [CrossRef] [Google Scholar]

4. O'Connor S, Campbell R, Cortez H, Knowles T. Whale watching worldwide: tourism numbers, expenditures and economic benefits. Yarmouth MA, Us: prepared by Economists at Large; 2009.

v. Balmford A, Beresford J, Green J, Naidoo R, Walpole Chiliad, Manica A. A Global Perspective on Trends in Nature-Based Tourism. PLoS Biol. 2009;seven: e1000144 10.1371/journal.pbio.1000144 [PMC complimentary commodity] [PubMed] [CrossRef] [Google Scholar]

6. Wade AA, Theobald DM. Residential development encroachment on U.S. protected areas. Conserv Biol. 2010;24: 151–161. 10.1111/j.1523-1739.2009.01296.x [PubMed] [CrossRef] [Google Scholar]

7. Wittemyer K, Elsen P, Bean WT, Burton ACO, Brashares JS. Accelerated human population growth at protected area edges. Science. 2008;321: 123–126. x.1126/science.1158900 [PubMed] [CrossRef] [Google Scholar]

8. Naughton-Treves L, Holland MB, Brandon K. The role of protected areas in conserving biodiversity and sustaining local livelihoods. Annu Rev Environ Resour. 2005;30: 219–252. [Google Scholar]

nine. Reed SE, Merenlender AM. Quiet, nonconsumptive recreation reduces protected area effectiveness. Conserv Lett. 2008;1: 146–154. [Google Scholar]

10. Eagles PFJ, McCool, Stephen F, Haynes CD, Un Environment Program, World Tourism Organization, International Union for Conservation of Nature and Natural Resource. Sustainable tourism in protected areas: guidelines for planning and management Gland, Switzerland: IUCN—the Globe Conservation Marriage; 2002. [Google Scholar]

eleven. IUCN, UNEP. The Globe Database on Protected Areas (WDPA) [Internet]. Cambridge, UK: UNEP-WCMC; 2014. Bachelor: www.protectedplanet.net [Google Scholar]

12. Becken Due south, Job H. Protected areas in an era of global-local change. J Sustain Tour. 2014;22: 507–527. [Google Scholar]

13. McCurdy LE, Winterbottom KE, Mehta SS, Roberts JR. Using nature and outdoor activity to ameliorate children's wellness. Curr Probl Pediatr Adolesc Health Care. 2010;40: 102–117. ten.1016/j.cppeds.2010.02.003 [PubMed] [CrossRef] [Google Scholar]

14. Louv R. Last child in the woods: Saving our children from nature-arrears disorder Algonquin Books; 2005. [Google Scholar]

15. Bushell R, Eagles PFJ. Tourism and protected areas: benefits beyond boundaries: the Vth IUCN World Parks Congress CABI; 2007. [Google Scholar]

16. Zhong L, Buckley RC, Wardle C, Wang L. Environmental and visitor management in a thousand protected areas in People's republic of china. Biol Conserv. 2015;181: 219–225. [Google Scholar]

17. Zaradic PA, Pergams ORW, Kareiva P. The impact of nature experience on willingness to support conservation. PLoS ONE. 2009;4: e7367 10.1371/journal.pone.0007367 [PMC gratuitous article] [PubMed] [CrossRef] [Google Scholar]

18. Losos E, Hayes J, Phillips A, Wilcove D, Alkire C. Taxpayer-Subsidized Resource Extraction Harms Species. BioScience. 1995;45: 446–455. [Google Scholar]

19. Steven R, Castley JG. Tourism as a threat to critically endangered and endangered birds: global patterns and trends in conservation hotspots. Biodivers Conserv. 2013;22: 1063–1082. [Google Scholar]

20. Mainini B, Neuhaus P, Ingold P. Behaviour of marmots marmota marmota under the influence of different hiking activities. Biol Conserv. 1993;64: 161–164. [Google Scholar]

21. Naylor LM, J. Wisdom Yard, G. Anthony R. Behavioral responses of N American elk to recreational activity. J Wildl Manag. 2009;73: 328–338. [Google Scholar]

22. George SL, Crooks KR. Recreation and large mammal activity in an urban nature reserve. Biol Conserv. 2006;133: 107–117. [Google Scholar]

23. Rogala JK, Hebblewhite Thousand, Whittington J, White CA, Coleshill J, Musiani M. Human action differentially redistributes large mammals in the Canadian Rockies national parks. Ecol Soc. 2011;16. [Google Scholar]

24. Banks PB, Bryant JV. 4-legged friend or foe? Domestic dog walking displaces native birds from natural areas. Biol Lett. 2007;3: 611–613. x.1098/rsbl.2007.0374 [PMC free article] [PubMed] [CrossRef] [Google Scholar]

25. Heil L, Fernandez-Juricic E, Renison D, Cingolani AM, Blumstein DT. Avian responses to tourism in the biogeographically isolated high Cordoba Mountains, Argentine republic. Biodivers Conserv. 2007;sixteen: 1009–1026. [Google Scholar]

26. Arlettaz R, Patthey P, Baltic Chiliad, Leu T, Schaub M, Palme R, et al. Spreading Complimentary-Riding Snow Sports Represent a Novel Serious Threat for Wildlife. Proc Biol Sci. 2007;274: 1219–1224. ten.1098/rspb.2006.0434 [PMC free article] [PubMed] [CrossRef] [Google Scholar]

27. Müllner A, Eduard Linsenmair G, Wikelski M. Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol Conserv. 2004;118: 549–558. [Google Scholar]

28. Beale CM, Monaghan P. Modeling the furnishings of limiting the number of visitors on failure rates of seabird nests. Conserv Biol. 2005;xix: 2015–2019. [Google Scholar]

29. Finney SK, Pearce-Higgins JW, Yalden DW. The result of recreational disturbance on an upland breeding bird, the golden plover Pluvialis apricaria. Biol Conserv. 2005;121: 53–63. [Google Scholar]

30. Kangas K, Luoto M, Ihantola A, Tomppo E, Siikamäki P. Recreation-induced changes in boreal bird communities in protected areas. Ecol Appl. 2010;20: 1775–1786. [PubMed] [Google Scholar]

31. Riffell SK, Gutzwiller KJ, Anderson SH. Does Repeated Human Intrusion Crusade Cumulative Declines in Avian Richness and Abundance? Ecol Appl. 1996;6: 492–505. [Google Scholar]

32. Frid A, Dill LM. Human-acquired disturbance stimuli as a course of predation risk. Conserv Ecol. 2002;6: xi. [Google Scholar]

33. Boyle SA, Samson FB. Furnishings of Nonconsumptive Recreation on Wild animals: A Review. Wildl Soc Bull. 1985;thirteen: 110–116. [Google Scholar]

34. Duffus DA, Dearden P. Non-consumptive wild fauna-oriented recreation: A conceptual framework. Biol Conserv. 1990;53: 213–231. [Google Scholar]

35. Knight RL, Gutzwiller K. Wild fauna and Recreationists: Coexistence Through Management And Inquiry. Isle Printing; 1995. [Google Scholar]

36. Pomerantz GA, Decker DJ, Goff GR, Purdy KG. Assessing Bear on of Recreation on Wildlife: A Classification Scheme. Wildl Soc Balderdash. 1988;16: 58–62. [Google Scholar]

37. Barros A, Monz C, Pickering C. Is tourism damaging ecosystems in the Andes? Current cognition and an agenda for future research. AMBIO. 2014; 1–17. [PMC free article] [PubMed] [Google Scholar]

38. Marzano M, Dandy N. Recreationist behaviour in forests and the disturbance of wild animals. Biodivers Conserv. 2012;21: 2967–2986. [Google Scholar]

39. Sato CF, Wood JT, Lindenmayer DB. The effects of winter recreation on tall and subalpine brute: A systematic review and meta-assay. Lindborg R, editor. PLoS 1. 2013;8: e64282 x.1371/periodical.pone.0064282 [PMC free article] [PubMed] [CrossRef] [Google Scholar]

40. Gallagher AJ, Vianna GMS, Papastamatiou YP, Macdonald C, Guttridge TL, Hammerschlag N. Biological furnishings, conservation potential, and research priorities of shark diving tourism. Biol Conserv. 2015;184: 365–379. [Google Scholar]

41. Martínez-Abraín A, Oro D, Jiménez J, Stewart G, Pullin A. A systematic review of the effects of recreational activities on nesting birds of casualty. Basic Appl Ecol. 2010;11: 312–319. [Google Scholar]

43. Stankowich T. Ungulate flight responses to man disturbance: A review and meta-analysis. Biol Conserv. 2008;141: 2159–2173. [Google Scholar]

44. Steven R, Pickering C, Castley JG. A review of the impacts of nature based recreation on birds. J Environ Manage. 2011;92: 2287–2294. x.1016/j.jenvman.2011.05.005 [PubMed] [CrossRef] [Google Scholar]

45. Wolfe SA, Griffith B, Wolfe CAG. Response of reindeer and caribou to homo activities. Polar Res. 2000;19: 63–73. [Google Scholar]

46. Newsome D, Cole DN, Marion JL. Environmental impacts associated with recreational equus caballus-riding Environmental Impacts of Ecotourism. Cambridge: CABI Publishing; 2004. [Google Scholar]

47. Orams MB. Feeding wildlife as a tourism allure: a review of issues and impacts. Tour Manag. 2002;23: 281–293. [Google Scholar]

48. Parsons ECM. The Negative Impacts of Whale-Watching. J Mar Biol. 2012;2012: 1–9. [Google Scholar]

49. Pullin Equally, Knight TM. Doing more than expert than harm–Building an evidence-base for conservation and environmental management. Biol Conserv. 2009;142: 931–934. [Google Scholar]

50. Pullin AS, Stewart GB. Guidelines for Systematic Review in Conservation and Environmental Management. Conserv Biol. 2006;20: 1647–1656. 10.1111/j.1523-1739.2006.00485.ten [PubMed] [CrossRef] [Google Scholar]

51. Barto EK, Rillig MC. Dissemination biases in ecology: consequence sizes matter more than than quality. Oikos. 2012;121: 228–235. [Google Scholar]

52. Keller VE. Effects of human being disturbance on Eider ducklings somateria mollissima in an estuarine habitat in Scotland. Biol Conserv. 1991;58: 213–228. [Google Scholar]

53. Lortie CJ, Aarssen LW, Budden AE, Koricheva JK, Leimu R, Tregenza T. Publication bias and merit in ecology. Oikos. 2007;116: 1247–1253. [Google Scholar]

54. Jennions MD, Lortie CJ, Rosenberg MS, Rothstein 60 minutes. Publication and related biases In: Koricheva J, Gurevitch J, Mengersen 1000, editors. Handbook of Meta-analysis in Environmental and Evolution. Princeton, NJ: Princeton University Printing; 2013. [Google Scholar]

55. Koricheva J, Gurevitch J, Mengersen 1000, editors. Handbook of meta-analysis in ecology and evolution Princeton, NJ: Princeton Academy Press; 2013. [Google Scholar]

56. Steidl RJ, Anthony RG. Experimental Effects of Human Activeness on Breeding Baldheaded Eagles. Ecol Appl. 2000;10: 258–268. [Google Scholar]

57. IUCN. The IUCN Redlist of Threatened Species [Net]. 2015. Report No.: Version 2015.iv. Available: http://www.iucnredlist.org

58. McCullagh P. Regression Models for Ordinal Information. J R Stat Soc Ser B Methodol. 1980;42: 109–142. [Google Scholar]

lx. R Core Squad. R: a language and environs for statistical calculating Vienna, Republic of austria: R Foundation for Statistical Computing; 2015. [Google Scholar]

62. Bates D, Maechler One thousand, Bolker B, Walker Southward. Plumbing fixtures Linear Mixed-Furnishings Models Using lme4. J Stat Softw. 2015;67: one–48. [Google Scholar]

63. Pfeiffer S, Peter H-U. Ecological studies toward the management of an Antarctic tourist landing site (Penguin Isle, South Shetland Islands). Polar Rec. 2004;40: 345–353. [Google Scholar]

64. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GA, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403: 853–858. x.1038/35002501 [PubMed] [CrossRef] [Google Scholar]

66. Clark JA, May RM. Taxonomic Bias in Conservation Enquiry. Science. 2002;297: 191–192. [PubMed] [Google Scholar]

67. Welsh HH, Ollivier LM. Stream amphibians equally indicators of ecosystem stress: a case report from California's redwoods. Ecol Appl. 1998;8: 1118–1132. [Google Scholar]

68. Leighton PA, Horrocks JA, Kramer DL. Conservation and the scarecrow result: Can human activity do good threatened species by displacing predators? Biol Conserv. 2010;143: 2156–2163. [Google Scholar]

69. Monz CA, Pickering CM, Hadwen WL. Recent advances in recreation ecology and the implications of different relationships betwixt recreation use and ecological impacts. Front end Ecol Environ. 2013;11: 441–446. [Google Scholar]

70. Hawkins JP, Roberts CM, Hof Television receiver, Meyer KD, Tratalos J, Aldam C. Effects of Recreational Scuba Diving on Caribbean Coral and Fish Communities. Conserv Biol. 1999;13: 888–897. [Google Scholar]

71. Zakai D, Chadwick-Furman NE. Impacts of intensive recreational diving on reef corals at Eilat, northern Ruby-red Sea. Biol Conserv. 2002;105: 179–187. [Google Scholar]

72. Semeniuk CAD, Bourgeon Due south, Smith SL, Rothley KD. Hematological differences between stingrays at tourist and non-visited sites suggest physiological costs of wild fauna tourism. Biol Conserv. 2009;142: 1818–1829. [Google Scholar]

73. Semeniuk CAD, Rothley KD. Costs of group-living for a normally solitary forager: furnishings of provisioning tourism on southern stingrays Dasyatis americana. Mar Ecol Prog Ser. 2008;357: 271–282. [Google Scholar]

74. Marzluff JM, Neatherlin Due east. Corvid response to human settlements and campgrounds: Causes, consequences, and challenges for conservation. Biol Conserv. 2006;130: 301–314. [Google Scholar]

75. Jiménez M, Lemus JA, Meléndez 50, Blanco G, Laiolo P. Dampened behavioral and physiological responses mediate birds' clan with humans. Biol Conserv. 2011;144: 1702–1711. [Google Scholar]

76. Storch I, Leidenberger C. Tourism, mount huts and distribution of corvids in the Bavarian Alps, Germany. Wildl Biol. 2003;9: 301–308. [Google Scholar]

77. Gutzwiller KJ, Riffell SK, Anderson SH. Repeated Homo Intrusion and the Potential for Nest Predation by Grey Jays. J Wildl Manag. 2002;66: 372–380. [Google Scholar]

78. Cooper CA, Neff AJ, Poon DP, Smith GR. Behavioral Responses of Eastern Gray Squirrels in Suburban Habitats Differing in Homo Activity Levels. Northeast Nat. 2008;15: 619–625. [Google Scholar]

79. Griffin SC, Valois T, Taper ML, Scott Mills L. Furnishings of tourists on behavior and demography of olympic marmots. Conserv Biol. 2007;21: 1070–1081. 10.1111/j.1523-1739.2007.00688.x [PubMed] [CrossRef] [Google Scholar]

fourscore. Baudains TP, Lloyd P. Habituation and habitat changes tin moderate the impacts of human disturbance on shorebird convenance operation. Anim Conserv. 2007;x: 400–407. [Google Scholar]

81. Bejder L, Samuels A, Whitehead H, Gales Due north. Interpreting brusque-term behavioural responses to disturbance inside a longitudinal perspective. Anim Behav. 2006;72: 1149–1158. [Google Scholar]

82. Krebs J, Lofroth EC, Parfitt I. Multiscale Habitat Employ by Wolverines in British Columbia, Canada. J Wildl Manag. 2007;71: 2180–2192. [Google Scholar]

83. Malo J, Acebes P, Traba J. Measuring ungulate tolerance to human with flight distance: a reliable visitor management tool? Biodivers Conserv. 2011;20: 3477–3488. [Google Scholar]

84. Bejder L, Dawson SM, Harraway JA. Responses by Hector's Dolphins to Boats and Swimmers in Porpoise Bay, New Zealand. Mar Mammal Sci. 1999;fifteen: 738–750. [Google Scholar]

85. Steiner AJ, Leatherman SP. Recreational impacts on the distribution of ghost crabs Ocypode quadrata fab. Biol Conserv. 1981;20: 111–122. [Google Scholar]

86. Trip Northward van 5, Wiersma YF. A Comparison of All-Terrain Vehicle (ATV) Trail Impacts on Boreal Habitats Across Scales. Nat Areas J. 2015;35: 266–278. [Google Scholar]

87. Neumann W, Ericsson M, Dettki H. Does off-trail backcountry skiing disturb moose? Eur J Wildl Res. 2010;56: 513–518. [Google Scholar]

88. Thiel D, Jenni-Eiermann S, Braunisch Five, Palme R, Jenni Fifty. Ski tourism affects habitat use and evokes a physiological stress response in capercaillie Tetrao urogallus: a new methodological approach. J Appl Ecol. 2008;45: 845–853. [Google Scholar]

89. Billings WD. Arctic and Alpine Vegetations: Similarities, Differences, and Susceptibility to Disturbance. BioScience. 1973;23: 697–704. [Google Scholar]

90. Wildermuth RP, Anadón JD, Gerber LR. Monitoring behavior: assessing population status with rapid behavioral assessment. Conserv Lett. 2013;half-dozen: 86–97. [Google Scholar]

91. Gill JA, Norris K, Sutherland WJ. The Effects of Disturbance on Habitat Use by Blackness-Tailed Godwits Limosa limosa. J Appl Ecol. 2001;38: 846–856. [Google Scholar]

92. Bejder L, Samuels A, Whitehead H, Gales N, Isle of man J, Connor R, et al. Decline in relative affluence of bottlenose dolphins exposed to long-term disturbance. Conserv Biol. 2006;20: 1791–1798. 10.1111/j.1523-1739.2006.00540.x [PubMed] [CrossRef] [Google Scholar]

93. Guillemain Thou, Blanc R, Lucas C, Lepley M. Ecotourism disturbance to wildfowl in protected areas: historical, empirical and experimental approaches in the Camargue, Southern France. Biodivers Conserv. 2007;xvi: 3633–3651. [Google Scholar]

94. Medio D, Ormond RFG, Pearson M. Effect of briefings on rates of damage to corals past scuba divers. Biol Conserv. 1997;79: 91–95. [Google Scholar]

95. Acevedo-Gutiérrez A, Acevedo L, Boren L. Effects of the Presence of Official-Looking Volunteers on Harassment of New Zealand Fur Seals. Conserv Biol. 2011;25: 623–627. 10.1111/j.1523-1739.2010.01611.10 [PubMed] [CrossRef] [Google Scholar]

96. Cassini MH, Szteren D, Fernández-Juricic East. Argue furnishings on the behavioural responses of South American fur seals to tourist approaches. J Ethol. 2004;22: 127–133. [Google Scholar]

97. Ikuta LA, Blumstein DT. Practice fences protect birds from human disturbance? Biol Conserv. 2003;112: 447–452. [Google Scholar]

98. Cook CN, Possingham HP, Fuller RA. Contribution of Systematic Reviews to Management Decisions. Conserv Biol. 2013;27: 902–915. 10.1111/cobi.12114 [PMC free article] [PubMed] [CrossRef] [Google Scholar]

---

Articles from PLoS 1 are provided hither courtesy of Public Library of Science

---

chanimsed1988.blogspot.com

Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5145168/

Share this post