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474

Conservation Biology, Pages 474–487Volume 14, No. 2, April 2000

Single Species as Indicators of Species Richness and Composition in California Coastal Sage Scrub Birdsand Small Mammals

MARY K. CHASE*, WILLIAM B. KRISTAN III, ANTHONY J. LYNAM†, MARY V. PRICE, AND JOHN T. ROTENBERRY

Department of Biology and Center for Conservation Biology, University of California, Riverside, CA 92521, U.S.A.

Abstract:

Individual species may be useful as indicators of biodiversity if an association exists between thepresence of a species and another component of biodiversity. We evaluated 40 species of birds and smallmammals, including 11 species of conservation concern, as potential indicators of species richness and spe-cies composition in southern California coastal sage scrub habitats. This habitat, which is the target of large-scale conservation planning, has been greatly reduced by human development and supports many plantsand animals of conservation concern. We asked whether there is an association between the presence of a po-tential indicator species and the species richness and composition of the bird or small-mammal communityin which it is found. We used point counts and live-trapping to quantify the distribution of birds and smallmammals, respectively, at 155 points in 16 sites located in three counties. Of the few species we found associ-ated with species richness, some were associated with higher species richness and others with lower richness,and species of conservation concern were not more frequently associated with species richness than werecommon species. Ordination analysis revealed a geographic gradient in coastal sage scrub bird and small-mammal species composition across southern California, and 18 of the species we evaluated were associatedwith the composition of the bird and small-mammal community in which they were found. Our results sug-gest that efforts to conserve bird and small-mammal biodiversity in coastal sage scrub should not focus exclu-sively on rare species or on locations with the highest species richness, but instead should focus on a diversesuite of species that are representative of the range of variation in communities found in coastal sage scrubhabitats.

Especies Individuales como Indicadores de la Riqueza y la Composición de Especies de Aves y MamíferosPequeños en un Matorral Costero de Salvia en California

Resumen:

Especies individuales pueden ser utilizadas como indicadores de la biodiversidad si existe unaasociación entre la presencia de una especie y otro componente de la biodiversidad. Evaluamos 40 especiesde aves y mamíferos pequeños, incluyendo 11 especies de interés para la conservación como indicadores po-tenciales de la riqueza y la composición de especies en hábitats costeros de matorral de salvia del sur de Cal-ifornia. Ese hábitat, objeto de la planificación para la conservación a gran escala, ha sido ampliamente re-ducido debido al desarrollo humano y sirve de apoyo para muchas plantas y animales de interés para laconservación. Evaluamos si existe una asociación entre la presencia de una especie como potencial indica-dor y la riqueza y composición de especies de la comunidad de aves y mamíferos en las cuales se encuentra.Utilizamos puntos de conteo y trampeo de organismos vivos de aves y mamíferos pequeños respectivamentepara cuantificar la distribución en 155 puntos en 16 sitios localizados en tres condados. De las pocas espe-cies que encontramos asociadas con la riqueza de especies, algunas estuvieron asociadas con una riqueza deespecies alta y otras con una riqueza de especies baja, y las especies de interés para la conservación no estu-

*

email [email protected]

†

Current address: Wildlife Conservation Society, Box 170, Laksi, Bangkok 10210, ThailandPaper submitted June 19, 1998; revised manuscript accepted July 21, 1999.

Conservation BiologyVolume 14, No. 2, April 2000

Chase et al. Coastal Sage Scrub Indicator Species

475

vieron frecuentemente más asociadas con la riqueza de especies que las especies comunes. Un análisis de or-denamiento revela un gradiente geográfico en la composición de aves y mamíferos pequeños en las comu-nidades costeras de matorral de salvia a lo largo del sur de California, y 18 de las especies evaluadasestuvieron asociadas con la composición de las comunidades de aves y mamíferos pequeños en las cuales fu-eron encontradas. Nuestros resultados sugieren que los esfuerzos para la conservación de la biodiversidad deaves y mamíferos pequeños en matorral de salvia costero no se deberían enfocar exclusivamente en las espe-cies raras ni en las localidades con la mayor riqueza de especies, sino que deberán enfocarse en un grupo di-verso de especies que son representativas del rango de variación en las comunidades que se encuentran en

los hábitats costeros de matorral de salvia.

Introduction

The establishment of protected natural areas is oftennecessary for the in situ conservation of biodiversity inthreatened habitats (Soulé 1991). Because the amount ofhabitat that can be protected is usually limited, design-ers of reserve systems must prioritize the conservationvalue of potential reserves (Margules & Usher 1981;Usher 1986; Pressey et al. 1993; Williams et al. 1996).Biodiversity is a commonly used criterion for selectingreserves, and potential reserves can be evaluated formultiple levels of biological diversity, including geneticdiversity, species diversity, and community diversity(Noss 1990). This assessment would be simplified if biol-ogists could identify relatively easily measured indicatorsof biodiversity. A commonly used approach is the indi-cator species, defined by Landres et al. (1988) as “anorganism whose characteristics, such as presence or ab-sence, population density, dispersion, reproductive suc-cess, are used as an index of attributes too difficult, in-convenient, or expensive to measure.”

Many recent studies of biodiversity indicator taxa havefocused on whether patterns of species richness or rar-ity are correlated among taxa or whether areas withlarge numbers of rare species are also rich in species (e.g.,Ryti 1992; Kerr 1997; Prendergast & Eversham 1997; Law-ton et al. 1998; Pearson & Carroll 1998; Tardif & Des-Granges 1998; Troumbis & Dimitrakopoulos 1998; alsoreviewed in McGeoch 1998). Less often addressed iswhether the presence of an individual species in a po-tential reserve can serve as an indicator of species rich-ness or species composition (Launer & Murphy 1994;Nilsson et al. 1995; Niemi et al. 1997). Although criti-cism of the indicator species concept has led to grow-ing interest in habitat-based, multi-species conservationplanning (Beatley 1994; Martin 1994), single species re-main important foci of conservation efforts because theyare easier to identify and study than other levels of biodi-versity and are more likely to be protected by law (Noss1990; Martin 1994). For an individual species to be usedas an indicator, its distribution must provide relevant in-formation, for example, about the distributions of otherspecies. We define

biodiversity indicator species

as

those whose presence is correlated with high speciesrichness or with the presence of a threatened biologicalcommunity or subassociation.

Coastal sage scrub habitat in Southern California pro-vides an excellent testing ground for the use of indicatorspecies in conservation planning. Coastal sage scrub,which has been reduced to 10–30% of its former extentby conversion for human use, supports approximately100 animal and plant species considered rare, sensitive,threatened, or endangered by California or U.S. federalwildlife agencies (Atwood 1993; McCaull 1994). Califor-nia’s Natural Community Conservation Planning (NCCP)program aims to design a reserve system to protect bio-diversity in coastal sage scrub habitat while allowingeconomic development in areas of lower biological sig-nificance (Atwood 1993; McCaull 1994). The NCCP pro-gram has evolved largely in response to the legal pro-tection given to one coastal sage scrub species, theCalifornia Gnatcatcher (

Polioptila californica

). Planningdecisions have emphasized the conservation of this andother target species (Atwood 1993; State of California1993

a

; Atwood & Noss 1994). Therefore, it is importantto understand the relationship between the distributionof individual species and the overall patterns of biodiver-sity within coastal sage scrub habitat.

We used data from surveys of passerine birds andsmall mammals to evaluate the relationship between po-tential indicator species and several attributes of thecoastal sage scrub community in which they were found.Specifically, we asked two questions: (1) Is there an as-sociation between the presence of a potential indicatorspecies and the species richness of the bird or small-mammal community in which it was found? This mightbe true if, for example, a single rare species tends to oc-cur in species-rich sites. (2) Is there an association be-tween the presence of a potential indicator species andthe species composition of the bird and small-mammalcommunity in which it was found? If so, and if speciescomposition varies within coastal sage scrub habitat,then indicator species could be used to help ensure thatthis variation would be represented in a reserve system.In addition, we asked if patterns of species richness andcomposition in birds and small mammals are correlated.

476

Coastal Sage Scrub Indicator Species Chase et al.


Methods

Focal Species

We chose two groups of taxa as potential indicators inour analyses: (1) species or subspecies of conservationconcern (i.e., those identified as sensitive, threatened,or endangered, or suggested as targets of conservationplanning) and (2) species occurring commonly in oursamples (Table 1). The first group includes 11 taxa thathave been listed as species or subspecies of special con-cern by the California Department of Fish and Game(State of California 1992, 1993

b

) and three taxa that have

been suggested as foci of conservation efforts in River-side County because they occur at low densities (Anony-mous 1994). The second group includes species detectedat

.

10% and

,

90% of our sampling points, because spe-cies found in fewer samples are less likely to be charac-teristic of coastal sage scrub habitat and because speciesfound in almost all samples cannot represent within-hab-itat variation in species richness or composition.

Study Area

Coastal sage scrub is a partially drought-deciduous shrub-land found in southwestern California and northwestern

Table 1. Species chosen for evaluation as potential indicators of species richness and species composition in coastal sage scrub habitat, and their frequency of occurrence among sampling points (

n

5

155), among sites (

n

5

16), and among sites with

$

10 points (

n

5

9).

Number of detections

SpeciesSpecies code points sites

sites with

$

10 points

California Quail (

Callipepla

californica

) CAQU 80 16 9Mourning Dove (

Zenaida macroura

) MODO 85 15 9Greater Roadrunner (

Geococcyx californianus

)

a

GRRO 8 4 3Anna’s Hummingbird (

Calypte anna

) ANHU 51 13 8Costa’s Hummingbird (

Calypte costae

) COHU 93 16 9Horned Lark (

Eremophila alpestris

)

b

HOLA 3 1 1Western Scrub-Jay (

Aphelocoma californica

) SCJA 43 12 7Bushtit (

Psaltriparus minimus

) BUSH 91 15 8House Wren (

Troglodytes aedon

) HOWR 19 7 6Bewick’s Wren (

Thryomanes bewickii

) BEWR 115 16 9Canyon Wren (

Catherpes mexicanus

)

a

CANW 14 3 1Rock Wren (

Salpinctes obsoletus

)

a

ROWR 13 4 2Cactus Wren (

Campylorhynchus brunneicapillus

)

b

CACW 40 6 5Wrentit (

Chamaea fasciata

) WREN 108 14 8California Gnatcatcher (

Polioptila californica

)

b

CAGN 19 7 6Northern Mockingbird (

Mimus polyglottos

) NOMO 63 12 9California Thrasher (

Toxostoma redivivum

) CATH 76 15 9Loggerhead Shrike (

Lanius ludovicianus

)

b

LOSH 1 1 1Orange-crowned Warbler (

Vermivora celata

) OCWA 24 9 7Common Yellowthroat (

Geothlypis trichas

) COYE 23 8 6Western Meadowlark (

Sturnella neglecta

) WEME 45 8 6White-crowned Sparrow (

Zonotrichia leucophrys

) WCSP 46 12 8Sage Sparrow (

Amphispiza belli

)

b

SAGS 37 8 4Black-chinned Sparrow (

Spizella atrogularis

) BCSP 64 10 6Rufous-crowned Sparrow (

Aimophila ruficeps

)

b

RCSP 89 15 9Song Sparrow (

Melospiza melodia

) SOSP 41 14 8Black-headed Grosbeak (

Pheucticus melanocephalus

) BHGR 18 5 3House Finch (

Carpodacus mexicanus

) HOFI 59 14 9Lesser Goldfinch (

Carduelis psaltria

) LEGO 49 14 7Pacific kangaroo rat (

Dipodomys agilis

) DIAG 43 8 4Stephens’ kangaroo rat (

Dipodomys stephensi

)

b

DIST 1 1 1Dulzura pocket mouse (

Chaetodipus californicus femoralis

)

b

CHCA 4 2 1San Diego pocket mouse (

Chaetodipus fallax fallax

)

b

CHFA 58 10 5Los Angeles pocket mouse (

Perognathus longimembris brevinasus

)

b

PELO 1 1 1Dusky-footed woodrat (

Neotoma fuscipes

) NEFU 39 9 5San Diego woodrat (

Neotoma lepida intermedia

)

b

NELE 58 12 7California mouse (

Peromyscus californicus

) PECA 54 11 6Cactus mouse (

Peromyscus eremicus

) PEER 99 15 9Deer mouse (

Peromyscus maniculatus

) PEMA 46 8 4Western harvest mouse (

Reithrodontomys megalotis

) REME 17 10 8

a

Species suggested as foci of conservation planning (Anonymous 1994).

b

Species or subspecies of special conservation concern (State of California 1992, 1993

b

).



477

Baja California that is dominated by shrubs 0.5–2.0 min height (Westman 1981). Plant species compositionvaries within this broadly defined habitat, and there areseveral distinct types of coastal sage scrub (Westman1983; White & Padley 1997). Dominant shrubs includeCalifornia sagebrush (

Artemisia californica

), black sage(

Salvia mellifera

), white sage (

Salvia apiana

), Califor-nia encelia (

Encelia californica)

, brittlebush (

Enceliafarinosa

), and California buckwheat (

Eriogonum fascic-ulatum

; Westman 1981, 1983). Our study sites were lo-cated in Orange, Riverside, and San Diego Counties (Fig.1). We selected sites and sampling points based on thepresence of the above shrub species and the ability tosecure permission to access the site.

Sampling

In designing our sampling, we were faced with the clas-sic dilemma of the tradeoff between extensive versus in-tensive sampling. Following recommendations from Ralphet al. (1995), and considering our need to survey a broadregion, we traded exhaustive sampling at each point foran increase in the number of points and sites sampled.Therefore, our sampling was not meant to provide an

exhaustive count of the number of species present butrather to provide a relative index of species richness andcomposition.

We established 155 sampling points at 16 sites (Fig. 1).Within each site, we placed points systematically incoastal sage scrub habitat with the following constraints:points were at least 50 m from roads, trails, and eco-tones with other habitats, and points were at least 200 mapart to avoid sampling the same individual birds atmore than one point. A maximum of 20 points was es-tablished per site. In sites that were too small to contain20 points, we established as many points as possible.

We sampled birds by conducting two, 5-minute unlim-ited-radius counts at each point (Ralph et al. 1995), oneearly in the breeding season (19 March–1 May 1996) andone later in the season (3–25 May 1996). All birds de-tected from the point center were included, except forthose located in adjacent nonscrub habitat types or de-tected only flying overhead. Second visits to each sitewere made in the same order as first visits to ensure thateach site was sampled in both early and late spring. Toavoid observer bias, point counts were conducted byfour experienced observers, and each point was sam-pled by a different observer on the first and second visit.To avoid potential bias due to time of day and weatherconditions, we conducted point counts between sunriseand 5 hours after sunrise on mornings with no rain orstrong wind, and we reversed the order in which pointswere sampled within each site between the first and sec-ond visits to the site. Bird species not well sampled bypoint counts include flocking species and nocturnal spe-cies (Ralph et al. 1993).

Small mammals were sampled over 3 consecutive daysof trapping at each point. We used 16 Sherman live-trapsspaced 8 m apart in a 4

3

4 grid. Mammal trapping gridswere centered within 15 m of the point from whichbirds were sampled. Points were sampled between 7May 1996 and 27 June 1996. Three-day trapping periodswere chosen because longer-term trapping at a subset ofpoints showed that 90% of all species detected at eachtrapping point with a 7-day trapping period were de-tected by the third day (M.V.P., unpublished data). Be-cause small-mammal activity can be affected by moon-light (Price et al. 1984), trapping was not done for 2days before and after a full moon. Traps were baitedwith a mixture of rolled oats, peanut butter, and cornsyrup. Mammals were identified to species using keysderived from Ingles (1965) and Jameson and Peeters(1988). Sherman traps of the size used in this study (8

3

9

3

23 cm) are effective for detecting most groups of non-volant small mammals (

,

500 g; mainly rodents) that po-tentially occur in coastal sage scrub habitats, including mu-rids, heteromyids, cricetines, and microtines (M’Closkey1972; Meserve 1976; Price & Waser 1984; Salvioni & Lid-icker 1995). Our sampling method, however, was notgeared toward several species of small mammals that po-

Figure 1. Location of study sites in California. Site names (and number of sampling points) are as fol-lows: 1, University of California, Riverside (5); 2, Syca-more Canyon Park (5); 3, Lake Perris State Recre-ational Area (20); 4, Motte Rimrock Reserve (10); 5, Kabian Park (10); 6, Santa Margarita Ecological Re-serve (5); 7, Pamo Valley (4); 8, Black Canyon (5); 9, Wild Animal Park (8); 10, Sweetwater River National Wildlife Refuge (11); 11, Point Loma (10); 12, Torrey Pines State Park (8); 13, Rancho Mission Viejo (10); 14, Starr Ranch (18); 15, Sycamore Hills (10); 16, Limestone Canyon (16).

478

Coastal Sage Scrub Indicator Species Chase et al.


tentially occur in our study sites: gray shrew (

Notiosorexcrawfordi

), ornate shrew (

Sorex ornatus

), broad-footedmole (

Scapanus latimanus

), valley pocket gopher (

Tho-momys bottae

), and California ground squirrel (

Spermo-philus beecheyi

).

Analysis

Many studies of biodiversity focus on the species rich-ness of entire study sites, which is known to be influ-enced by site characteristics such as area and habitatheterogeneity (e.g., Soulé et al. 1988). To focus on pat-terns of alpha diversity in coastal sage scrub rather thanpatterns associated with variation in area among sites,we instead analyzed species richness and composition atindividual sampling points. We evaluated (1) whetherthe presence of a potential indicator at certain pointswas associated with the species richness or compositionat those points, and (2) whether the presence of a po-tential indicator at certain sites was associated with therichness or composition averaged over all points withinthose sites.

Species Richness at Point and Site Scales

To determine if the presence of a focal species was anindicator of species richness, we first compared speciesrichness among individual sampling points (

n

5

155).We estimated species richness as the number of speciesdetected per point over the two sampling intervals, ex-cluding the focal species that was the subject of the test.Bird and mammal species richness were analyzed sepa-rately. Because our analyses were repeated for each fo-cal species, we used the standard Bonferroni correctionfor multiple tests to keep the table-wide Type I errorrate at 0.05. For all point-scale analyses, we tested 37 fo-cal species (

a

5

0.0014).Randomization tests (Sokal & Rohlf 1995) were used

to compare mean species richness at points where a fo-cal species was detected to the expected species rich-ness at a random sample of points. We used this as an al-ternative to a parametric test because the number ofpoints at which a focal species is found can be muchsmaller (or much larger) than the number of pointswhere it is not found (e.g., California Gnatcatchers weredetected at 19 out of 155 points). In this procedure, themean species richness (excluding the focal species) wascalculated from a random sample of points drawn fromthe 155 observed richness values, where the size of therandom sample equaled the number of points at whichthe focal species was detected. This procedure was iter-ated 10,000 times to create an expected distribution ofsample means. The observed mean species richness atpoints where the focal species was detected was com-pared to this distribution, and its statistical significance(departure from the expected mean) was determined.

We also compared species richness at sites where a fo-cal species was detected to sites where it was not de-tected. The mean number of species detected per pointdiffers significantly among sites (Chase et al. 1998). Wewished to determine whether this variation among sitesin the number of species detected per point was corre-lated with the distribution of any of our focal species. Tomaintain relatively uniform sample sizes across sites andto avoid sites with a small number of points, we restrictedthis analysis to sites with 10 or more points (

n

5

9). Wedid not test focal species that were detected at only onesite or that were absent from only one site (Table 1). Wetested 19 focal species (

a

5

0.0026). To compare meanspecies richness between sites with and without each ofthe focal species, we used a one-way analysis of variance(ANOVA). The ANOVAs were performed with STATAstatistical software (Stata Corporation 1997).

Species Composition

Species composition was analyzed by detrended corre-spondence analysis (DCA) based on species presence orabsence at each point and was conducted with PC-ORDstatistical software (McCune & Mefford 1995). The DCAis an ordination technique that quantifies the relation-ship among a set of points based on the similarity oftheir species composition, and the relationship amongspecies based on the similarity of their distributionamong points (Gauch 1982). Points and species are or-dered on axes so that points with similar species compo-sition will have similar axis scores, and species with sim-ilar patterns of distribution will also have similar scores.Thus, the scores of points on ordination axes can beused as an index of the species composition at thosepoints, and the mean scores of points within a site canbe used as an index of the species composition at a site.A further advantage is that DCA axes are linearized suchthat beta diversity (the compositional difference be-tween two points) is constant. Thus, a unit differencebetween two points at one end of a gradient representsthe same compositional change as a unit difference be-tween two points at the other end. Patterns of speciescomposition in birds and mammals were similar whenanalyzed separately, so we present results from a singleDCA analysis of both bird and mammal species.

We compared species composition at points where fo-cal species were detected to the expected species com-position at a random sample of points using a random-ization test of point scores on the first DCA axis. Withthe Bonferroni correction, the alpha level for each testwas 0.0014. To compare species composition betweensites with and without each of the focal species, we con-ducted a one-way ANOVA on the mean of the DCA axis-1 point scores for each site. We did not test focal speciesdetected at only one site or absent from only one site.The alpha level for each test was 0.0026. We examined



479

the relationship between species composition and geo-graphical location of our sampling points with a multi-ple linear regression of the DCA axis-1 point scores, us-ing as independent variables the Universal TransverseMercator (UTM) eastings and northings and the interac-tion of eastings and northings. For illustrative purposes,geographic contours of DCA axis-1 scores were esti-mated by an inverse distance weighting method ( JandelScientific 1994). In this method, values at all sampledpoints are used in interpolating contour intervals but areweighted inversely to their distance to each map point.

Results

Species Richness

On average, 12 bird species (range, 5–19) and 3 mam-mal species (range, 0–6) were detected at each samplingpoint. Bird and mammal species richness were not cor-related among points (r 5 0.05, p 5 0.64). Two speciesof conservation concern, the Loggerhead Shrike andStephens’ kangaroo rat, were detected at only one sam-pling point and thus could not be used in the point-scaleanalyses as focal species. Of the other potential indicatorspecies, only Sage Sparrows were associated with spe-cies richness at points where they were detected (n 537 points). At these points, the number of co-occurringbird species was 10.4 on average, compared to 11.7 spe-cies at randomly sampled points ( p , 0.0014). Themean mammal species richness at points where SageSparrows were detected was 3.6, compared with 2.8 atrandomly sampled points ( p , 0.0014).

The mean number of bird species detected per pointalso varied among sites, ranging from 9.0 at Point Lomato 13.4 at Limestone Canyon. The mean number ofmammal species detected per point ranged from 1.8 atPoint Loma and Rancho Mission Viejo to 4.8 at MotteRimrock. Bird and mammal species richness were notcorrelated among sites (r 5 0.08, p 5 0.84). Nine poten-tial indicator species were detected at all nine sites andtherefore could not be analyzed as indicators at the sitescale; also not analyzed at the site scale were 12 speciesfound at only one or at all but one site (Table 1). Of theremaining 19 species, only Common Yellowthroats wereassociated with higher bird species richness at sites wherethey were found (mean 5 12.6 at three sites whereCommon Yellowthroats were found; mean 5 9.9 at siteswhere they were not found; F 5 38.77, p 5 0.0004).The Western Scrub-Jay was associated with lower mam-mal species richness (mean 5 2.3 at seven sites whereWestern Scrub-Jays were found; mean 5 4.3 at siteswhere they were not found; F 5 26.38, p 5 0.0013). Al-though the results were not statistically significant, sev-eral other species tended to be associated with speciesrichness at sites where they were found: Greater Road-

runner (mean 5 3.6 mammal species at three sites wherethey were found; mean 5 2.4 at sites where they werenot found; F 5 4.28, p 5 0.08), San Diego pocket mice(mean 5 10.9 bird species at five sites where they werefound; mean 5 13.1 at sites where they were not found;F 5 7.54, p 5 0.03), dusky-footed woodrat (mean 5 1.9mammal species at five sites where they were found;mean 5 3.3 at sites where they were not found; F 55.65, p 5 0.05), California mouse (mean 5 1.9 mammalspecies at six sites where they were found; mean 5 3.6at sites where they were not found; F 5 9.14, p 5 0.02).

Species Composition

The first two DCA axes explained 44.9% of the covaria-tion in sample and species dispersion (axis-1 eigenvalue 50.313; axis-2 eigenvalue 5 0.136). The distribution ofpoints (classed by their approximate location) with re-spect to DCA axis 1 suggests that this axis might repre-sent geographic variation in species composition (Fig. 2).This is confirmed by a statistically significant multiple re-gression of DCA axis-1 point scores on UTM east and northcoordinates and their interaction (F 3,151 5 84.18, p ,0.001). This regression accounted for 62.6% of the totalvariation in DCA axis-1 scores. Each term in the regres-sion equation was significant (all p , 0.01). The geograph-ical nature of this variation was revealed when we plottedcontours of DCA axis-1 scores on a regional map (Fig. 3).

Of the 37 species we evaluated, seven birds and threemammals were significantly associated with points char-acterized by an “inland” species association, whereas sixbirds and two mammals were found at points with amore “coastal” species association (Table 2; Fig. 4). Theremaining 19 species occurred at points with a speciescomposition that was not significantly different from

Figure 2. Detrended correspondence analysis (DCA) ordination of 155 Californian coastal sage scrub sam-pling points based on presence or absence of 59 bird and 13 mammal species. Axes are DCA scores 3 100.

480 Coastal Sage Scrub Indicator Species Chase et al.


that of randomly sampled points. Of the 14 species ofconservation concern, 9 were clearly associated with in-land points, 2 were associated with coastal points, and 3were intermediate (Fig. 5). Those species that occurredat only one point (LOSH, DIST, PELO) were “peripheral”in their distribution with respect to the ordination, sug-gesting that their apparent rarity was due to our sam-pling in a habitat that was marginal for them.

Although Canyon Wrens and Horned Larks were indi-cators of species composition at a point scale, theycould not be analyzed at the site scale because theywere each found at only one site. Of the 19 speciestested at the site scale, one bird and two mammals weresignificantly associated with sites with a more coastalspecies composition, whereas two birds and two mam-mals were associated with sites with a more inland spe-cies composition (Table 2; Fig 4). The gradient in spe-cies composition among sites can be described in moredetail when the species-by-site matrix is ordered by DCAaxis-1 scores, thus revealing where each species occursalong the gradient (Table 3). For some species the pat-tern was strong: three species associated with the inlandcommunity (Sage Sparrow, Pacific kangaroo rat, anddeer mouse) were detected only at sites lacking the twospecies associated most strongly with coastal sites (Cac-tus Wren and dusky-footed woodrat), and vice versa.

In addition, we identified a core group of speciesfound at all the sites we sampled (Table 3), which in-

cluded California Towhee, Spotted Towhee, Costa’sHummingbird, Bewick’s Wren, and California Quail. Al-though the species composition of sites in San Diegocounty was generally intermediate to that of coastal (Or-ange county) and inland (Riverside County) sites, we didnot find a group of species that was associated primarilywith the center of the gradient (Table 3). Instead, SanDiego sites (sites 7–12 in Table 3) tended to containboth species characteristic of inland sites, such as SageSparrow and San Diego pocket mouse, and species char-acteristic of coastal sites, such as Wrentit and Californiamouse.

Discussion

Species Richness

Three of the 37 species we tested were significantly as-sociated with species richness, and four additional spe-cies showed marginally nonsignificant associations. Inthree cases the presence of an individual species was as-sociated with higher species richness, whereas in fourcases it was associated with lower species richness. Spe-cies of conservation concern were not more frequentlyassociated with species richness than were commonspecies. Therefore, species of conservation concern can-not be assumed to be indicators of “hotspots” of birdand small-mammal richness in coastal sage scrub.

Similarly, two recent studies show little geographicalcorrespondence between locations with high numbersof rare taxa and locations with high species richness(birds, Williams et al. 1996; birds, liverworts, and aquaticplants, Prendergast et al. 1993). In contrast, Debinskiand Brussard (1994) found an overlap between sites thatsupport high species diversity and sites that support rarespecies of birds and butterflies. The usefulness of rarespecies as indicators of species richness is likely to varyamong geographic locations and spatial scales (McGeoch1998).

In several cases the presence of a bird species was as-sociated with small-mammal richness or vice versa, sug-gesting that single species could potentially serve ascross-taxa indicators. But the overall lack of correlationbetween bird and mammal species richness in our studysuggests that there is no substitute for targeting multipletaxa in conservation planning. Similarly, several otherstudies show few consistent relationships between spe-cies richness in different taxa (butterflies and plants, Kre-men 1992; six vertebrate taxa, Lombard 1995; birds, but-terflies, and dragonflies and damselflies, Prendergast &Eversham 1997; birds, butterflies, and six invertebratetaxa, Lawton et al. 1998). One study, which took placeon a global scale, shows a correlation among speciesrichness in tiger beetles, birds, and butterflies (Pearson &Cassola 1992). These results also suggest that the useful-

Figure 3. Contours of detrended correspondence anal-ysis (DCA) scores of 155 Californian coastal sage scrub sampling points. Points overlap on map due to their proximity to one another within sites. Numbers are DCA scores 3 100.


Chase et al. Coastal Sage Scrub Indicator Species 481

ness of biodiversity indicators varies among spatialscales (Flather et al. 1997; Reid 1998).

Species Composition

Ordination analysis (DCA) revealed a geographic gradientbird and small-mammal species composition in coastalsage scrub across southern California (Figs. 2 & 3). A sim-ilar coastal-inland gradient has been found in the coastalsage scrub plant community at our sampling points( J.T.R., unpublished data). Also, classification analysesof coastal sage scrub vegetation types (Westman 1983) dis-tinguish between a coastal species association (Diegan)and a higher-elevation inland species association (River-sidian). Underlying the vegetation gradient is a strongclimatic gradient, with the inland area experiencinghigher evapotranspiration during the summer than thecoastal area (Westman 1981). If, as this suggests, parallelgeographic variation exists in the species compositionof bird, small-mammal, and plant communities in coastalsage scrub, then individual species or groups of speciesin one taxon might be useful as indicators of species as-semblages in other taxa.

Eighteen of the species we evaluated were associatedwith the composition of the bird and small-mammalcommunity in which they were found (Table 2). In par-ticular, the Cactus Wren, dusky-footed woodrat, and Cal-

ifornia mouse were strongly associated with a morecoastal-type bird and small-mammal community at boththe point and site scales. Of these three, the CactusWren has two advantages as a biodiversity indicator spe-cies: it is more easily detected than the small-mammalspecies, and it is a species of special conservation con-cern. The Greater Roadrunner, Sage Sparrow, Pacifickangaroo rat, and deer mouse were the species moststrongly associated with a more inland-type bird andsmall-mammal community at both spatial scales. TheSage Sparrow, a species of conservation concern, is alsoassociated with low bird species richness and high mam-mal species richness.

Several species significantly associated with speciescomposition at the point scale were not significant atthe site scale (Table 2). For some species, such as theWestern Scrub-Jay and the San Diego pocket mouse, thismay be due to the reduced power of the site-scale tests.Other species, however, such as the Black-chinned Spar-row and the Rufous-crowned Sparrow, appear to havebeen associated with a distinct species assemblage at thepoint scale but not at the larger spatial scale of sites.These species were widely distributed among sites, butwithin sites they occurred primarily in a subset of pointswith a distinct species assemblage. For example, al-though the Rufous-crowned Sparrow was found at 15out of 16 sites, it was strongly associated with points

Table 2. Results of analyses testing single species as potential indicators of bird and small mammal species composition.a

Point scale Site scale

Speciesb

mean DCA axis-1score of pointswhere detectedc pd

mean DCA axis-1score for sites

where detected

mean DCA axis-1score for sites

where not detected pe

Black-chinned Sparrow 84.6 ,0.0002 108.5 100.0 .0.8Cactus Wren f 65.6 ,0.0002 58.0 166.0 ,0.002*Canyon Wren f 199.0 ,0.0002Greater Roadrunner f 179.9 ,0.0008 187.2 65.4 ,0.0001*Horned Lark f 249.7 ,0.0002House Wren 46.8 ,0.0002 78.8 160.5 .0.06Orange-crowned Warbler 65.5 ,0.0003 99.0 130.3 .0.5Rufous-crowned Sparrow f 131.4 ,0.0006Rock Wren f 186.9 ,0.0002 121.4 101.6 .0.07Sage Sparrow f 179.5 ,0.0001 166.0 58.0 ,0.002*Western Scrub-Jay 56.3 ,0.0001 85.1 179.3 .0.05Western Meadowlark 172.4 ,0.0001 119.9 78.1 .0.3Wrentit 73.7 ,0.0001Pacific kangaroo rat 173.3 ,0.0001 166.0 58.0 ,0.002*San Diego pocket mouse f 161.2 ,0.0001 148.8 52.5 .0.01Dusky-footed woodrat 54.7 ,0.0001 58.0 166.0 ,0.002*California mouse 57.0 ,0.0001 65.4 187.2 ,0.0001*Deer mouse 173.4 ,0.0001 166.0 58.0 ,0.002*aPoints where potential indicator species were detected were compared to random points (n 5 155 points), and points within sites where poten-tial indicator species were detected were compared to points within sites where they were not detected (n 5 9 sites).bOnly species with significant associations at the point or site scale are included. See Table 1 for scientific names.cMean DCA axis-1 score of all points, 108.8.dValues from randomization test; all are statistically significant.eValues from analysis of variance; statistically significant values are marked with an asterisk.fSpecies of conservation concern.



where the species composition was more typical of in-land sites. This suggests that the variation we found inbird and mammal species composition may be associ-ated with variation in habitat characteristics within sites,as well as with larger-scale geographic variation. This isconsistent with what is known about variation in thecoastal sage scrub plant community. For example, DeSi-mone and Burk (1992) found small-scale variation inplant species associations within the Starr Ranch sitethat paralleled regional-scale variation.

The two mammals associated with the coastal speciesassemblage, the dusky-footed woodrat and Californiamouse, were also associated with low small-mammalspecies richness, and two of the species associated withthe inland species assemblage, the Sage Sparrow and SanDiego pocket mouse, were associated with low bird-spe-cies richness. This suggests that a reserve system encom-passing the range of variation in coastal sage scrub birdand small-mammal communities must include sites withboth high and low species richness.

Other Uses of Indicators

Single species may also be used as indicators of environ-mental change—for example, to detect environmentalcontamination, to evaluate the effects of changes in hab-itats over time, or to monitor population trends of otherspecies (Landres et al. 1988; Temple & Wiens 1989;Noss 1990), and for this purpose the evaluation criteriamay differ (e.g., Kremen 1992; Debinski & Brussard

1994; Lawton et al. 1998; McGeoch 1998; Rodríguez etal. 1998). Several of the species associated with speciescomposition in our study may also be useful as indica-tors of environmental change due to their sensitivity tohabitat fragmentation (Cactus Wren, Soulé et al. 1988;Sage Sparrows, Black-chinned Sparrows, Rufous-crownedSparrows, Bolger et al. 1997).

An additional group of species that may warrant spe-cial conservation effort are umbrella species—“specieswith large area requirements, which if given sufficientprotected habitat area, will bring many other species un-der their protection” (Noss 1990)—although large arearequirements per se do not ensure that co-occurringspecies will benefit from the protection of a single spe-cies (Landres et al. 1988). Of the species we evaluated,Greater Roadrunners are potential umbrella species withinthe inland-type species assemblage because of their largearea requirements (Hughes 1996). The California Gnat-catcher, which has been a major focus of conservationefforts in this region, was not an indicator either of com-munity composition or of species richness withincoastal sage scrub, although it may still be an indicatorof environmental change because of its sensitivity tohabitat fragmentation (Soulé et al. 1988) or an umbrellaspecies because of its large territory requirement (Fleuryet al. 1998; Preston et al. 1998).

Caveats

Any sample that is not exhaustive will not detect all spe-cies present and thus will always underestimate truespecies richness at a point or other sampling unit. In our

Figure 4. Detrended correspondence analysis (DCA) ordination of bird and small-mammal species with statistically significant indicator species plotted. The ordination axes are the same as in Fig. 2. Species label is centered over species score. Asterisks indicate species of conservation concern. Species in italics were signifi-cant at the site scale as well as the point scale; other species significant only at point scale. See Table 1 and Appendix 1 for species codes.

Figure 5. Detrended correspondence analysis (DCA) ordination of bird and small-mammal species with species of conservation concern plotted. The ordina-tion axes are the same as in Fig. 2. Species label is cen-tered over species score (except for NELE). Species in italics were detected at only a single point. See Table 1 and Appendix 1 for species codes.



Table 3. Occurrences of species among study sites.*

Site SpeciesscoreSpecies 13 14 15 16 12 6 8 11 10 7 9 4 3 2 5 1

WAVI 1 2262WIWR 1 2262NUWO 1 1 1 2214LASP 1 2196PSFL 1 2190HOOR 1 2134OATI 1 1 1 1 1 1 2132SAPH 1 1 1 1 2125HOWR 1 1 1 1 1 1 1 2108ACWO 1 1 1 1 2103PHAI 1 1 1 1 1 287NEFU 1 1 1 1 1 1 1 1 1 285SCJA 1 1 1 1 1 1 1 1 1 1 1 1 283GRSP 1 1 1 1 1 279PECA 1 1 1 1 1 1 1 1 1 1 1 278RCKI 1 259CHCA 1 1 259BLPH 1 254CACW 1 1 1 1 1 1 251WIWA 1 1 1 1 1 1 1 248OCWA 1 1 1 1 1 1 1 1 1 243BHGR 1 1 1 1 1 242LAZB 1 1 1 1 1 1 1 224WREN 1 1 1 1 1 1 1 1 1 1 1 1 1 1 220NOFL 1 1 1 1 1 1 1 216ATFL 1 1 1 1 210BCSP 1 1 1 1 1 1 1 1 1 1 19CATH 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 62MODO 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 79SPTO 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 82AMGO 1 87COHU 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 92ANHU 1 1 1 1 1 1 1 1 1 1 1 1 1 93COBU 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 93NELE 1 1 1 1 1 1 1 1 1 1 1 1 95REME 1 1 1 1 1 1 1 1 1 1 97CAKI 1 107COYE 1 1 1 1 1 1 1 1 107BEWR 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 123LEGO 1 1 1 1 1 1 1 1 1 1 1 1 1 1 124CALT 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 125PEER 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 131NOMO 1 1 1 1 1 1 1 1 1 1 1 1 133CAQU 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 144BGGN 1 1 1 1 1 1 152EUST 1 1 1 1 1 157SOSP 1 1 1 1 1 1 1 1 1 1 1 1 1 1 159HOFI 1 1 1 1 1 1 1 1 1 1 1 1 1 1 179CAGN 1 1 1 1 1 1 1 208RCSP 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 215WCSP 1 1 1 1 1 1 1 1 1 1 1 1 273NOOR 1 1 1 277WEKI 1 1 1 291CHFA 1 1 1 1 1 1 1 1 1 1 292BHCO 1 297DIAG 1 1 1 1 1 1 1 1 303PEMA 1 1 1 1 1 1 1 1 303GRRO 1 1 1 1 310SAGS 1 1 1 1 1 1 1 1 311BRBL 1 312WEME 1 1 1 1 1 1 1 1 312

continued



analyses, however, we are concerned with comparativerather than absolute species richness. For our analysesto be biased with respect to richness, the species accu-mulation rates—the number of species added at a pointas survey effort increases—would have to differ system-atically among points, such that additional samplingwould change the rankings of points based on the num-ber of species detected. This is unlikely in our surveysbecause our sampling points were intentionally locatedin similar coastal sage scrub vegetation throughout thesurvey region. Another drawback of nonexhaustive sam-pling is that potential indicator species that are incon-spicuous may have been missed at individual points.Again, this would introduce a bias in our analyses only ifthe presence of a potential indicator was less likely to bedetected at points with a nonrandom species richness orcomposition.

Even if there is no systematic bias, however, randombetween-point error in estimating richness will remainin any nonexhaustive sampling effort. This source ofvariation reduced the power of our statistical tests andhence reduced our ability to identify species that areweak indicators (in statistical parlance, species associ-ated with a low effect size). It did not reduce our confi-dence in those species that the statistical tests had al-ready identified. Increasing the sampling effort at apoint, by reducing error variance, would likely yield ad-ditional statistically significant indicator species. Onemight argue, however, that because these additionalspecies are associated with small effect sizes, their use-fulness in a planning context is diminished compared tothat of the others already identified.

The issue of “undersampling” occurs with respect tocommunity composition as well. Again, however, unlessthere is some systematic bias across sites (e.g., if less-conspicuous species, which are undersampled in lessthan exhaustive surveys, occur nonrandomly with respectto species composition), our results should be robust. We

also have an independent assessment that indicates thatour estimate of community composition at a point is ro-bust. In the year preceding the collection of the data re-ported here (1995), we initiated a pilot effort in which wesampled birds and small mammals using the same tech-niques at 78 points distributed among eight sites. Of those78 points, 65 were in common with the 155 reportedhere. We performed a DCA of those 78 points and thencorrelated the 1995 DCA axis-1 scores of the 65 points incommon with their scores on the 1996 DCA axis 1. Ifpoint sampling inadequately captures composition—ifone were simply collecting a small, random subsample ofthe species occurring at each point—then one would ex-pect little association between the two scores. Instead,the correlation we found was highly statistically signifi-cant (r 5 0.88, df 5 63, p , 0.0001), implying a high sim-ilarity of species composition between years.

Conclusion

The presence of some individual species may serve as in-dicators of the overall species composition of birds andsmall mammals in a coastal sage scrub habitat patch butmay say less about its species richness. Therefore, to al-low the most effective use of individual species as tar-gets of conservation planning in coastal sage scrub, thelist of species should at least include those from bothends of the geographic spectrum of species composi-tion. Conservation efforts are particularly needed in in-land coastal sage scrub where the habitat is threatenedby air pollution and grazing, as well as by the more wide-spread threats of urbanization, increasing fire frequency,and invasion by exotic plants (Westman 1987; O’Leary1990; Minnich & Dezzani 1998). Ideally, future evalua-tions of indicator species in coastal sage scrub wouldinclude additional taxa, such as the bird and mammalspecies not sampled in our study and herptiles, inverte-brates, and plants. Even if certain individual species are

Table 3. (continued)

Species

Site Speciesscore13 14 15 16 12 6 8 11 10 7 9 4 3 2 5 1

ROWR 1 1 1 318RWBL 1 320CANW 1 1 1 330DEJU 1 330PELO 1 331MUMU 1 332MICA 1 1 333SAVS 1 339DIST 1 349HOLA 1 382LOSH 1 438Site Scores 40 52 58 60 67 72 75 80 102 109 111 176 182 198 203 205

*Species are ordered by their DCA axis-1 scores (3100), and sites are ordered by the mean axis-1 sample scores of their points (3100). Sitenumbers as in Fig. 1; species codes as in Table 1 and Appendix 1.



found to be reliable indicators of biodiversity, however,more study is needed to show whether the protection ofan indicator will necessarily result in the protection ofother species sharing the same habitat. Efforts to con-serve the coastal sage scrub community should not fo-cus exclusively on rare species or on locations with thehighest species richness but instead should focus on adiverse suite of species representative of the range ofvariation found in coastal sage scrub habitats.

Acknowledgments

This study was funded by the California Department ofFish and Game and the U.S. Geological Survey, Biologi-cal Resources Division. We thank W. Tippitts, P. Stine,and S. Viers for administrative assistance. We are gratefulfor the excellent field work of P. Addison, D. Kristan, M.Misenhelter, M. A. Patten, L. Pagni, J. Ruvinsky, and P.Wellburn. We thank M. Bryant for writing the programfor the randomization test. Comments on an earlier ver-sion of the manuscript were provided by K. Ellison, M.Patten, M. Misenhelter, S. Henderson, K. Preston, S. Hejl,and two anonymous reviewers. We thank the followingindividuals and organizations for providing permissionfor us to work on lands they manage and/or for provid-ing logistical help: B. Carlson, P. DeSimone, G. Hund, D.Kamata, D. Lydy, M. Asam, L. Munoz, J. Opdycke, T.Smith, M. Sanderson, S. Shapiro, S. Weber, M. Wells, A.Yuen, the U.S. Forest Service, the Irvine Company, andthe Rancho Mission Viejo Company.

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Appendix 1Additional species detected at 155 sampling points and not evaluated as indicators, ordered from most to least frequently detected.

Common name Scientific nameNumberof points Species code

BirdsCalifornia Towhee Pipilo crissalis 145 CALTSpotted Towhee Pipilo maculatus 140 SPTONorthern Flicker Colaptes auratus 16 NOFLAcorn Woodpecker Melanerpes formicivorus 15 ACWOGrasshopper Sparrow Ammodramus savannarum 15 GRSPLazuli Bunting Passerina amoena 13 LAZBPhainopepla Phainopepla nitens 11 PHAIWilson’s Warbler Wilsonia pusilla 10 WIWABlue-gray Gnatcatcher Polioptila caerulea 9 BGGNOak Titmouse Parus inornatus 8 OATIAsh-throated Flycatcher Myiarchus cinerascens 6 ATFLEuropean Starling Sturnus vulgaris 6 EUSTSay’s Phoebe Sayornis saya 6 SAPHRed-winged Blackbird Agelaius phoeniceus 4 RWBLWestern Kingbird Tyrannus verticalis 4 WEKIBrewer’s Blackbird Euphagus cyanocephalus 3 BRBLBullock’s Oriole Icterus bullockii 3 BUORNuttall’s Woodpecker Picoides nuttallii 3 NUWOBrown-headed Cowbird Molothrus ater 2 BHCOAmerican Goldfinch Carduelis tristis 1 AMGOBlack Phoebe Sayornis nigricans 1 BLPHCassin’s Kingbird Tyrannus vociferans 1 CAKIDark-eyed Junco Junco hyemalis 1 DEJUHooded Oriole Icterus cucullatus 1 HOORLark Sparrow Chondestes grammacus 1 LASPPacific-slope Flycatcher Empidonax dificilis 1 PSFLRuby-crowned Kinglet Regulus calendula 1 RCKISavannah Sparrow Passerculus sandwichensis 1 SAVSWarbling Vireo Vireo altiloquus 1 WAVIWinter Wren Troglodytes troglodytes 1 WIWR

MammalsCalifornia vole Microtus californicus 3 MICAHouse mouse Mus musculus 1 MUMU

Documents

Single Species as Indicators of Species Richness and …public.csusm.edu/wkristan/chase_indicators.pdf · 2006-11-28 · Single Species as Indicators of Species Richness and Composition