Journal of Applied Ecology 2011, 48, 6775

doi: 10.1111/j.1365-2664.2010.01922.x

Modelling community dynamics based on species-level abundance models from detection nondetection data
Yuichi Yamaura1*, J. Andrew Royle2, Kouji Kuboi3, Tsuneo Tada3, Susumu Ikeno4 and Shunichi Makino1
Department of Forest Entomology, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan; 2U.S. Geological Survey, Patuxent Wildlife Research Center, Laurel, MD 20708, USA; 3 NPO School for Enjoying Nature in Forests, Mt. Sukegawa Preservatin Club, 4-12-18 Nishinarusawa-cho, Hitachi, Ibaraki 316-0032, Japan; and 4Ibaraki Branch, Wild Bird Society of Japan, 925-6 Nakagachichou, Mito, Ibaraki 310-0002, Japan
1

Summary 1. In large-scale eld surveys, a binary recording of each species detection or nondetection has been increasingly adopted for its simplicity and low cost. Because of the importance of abundance in many studies, it is desirable to obtain inferences about abundance at species-, functional group-, and community-levels from such binary data. 2. We developed a novel hierarchical multi-species abundance model based on species-level detection nondetection data. The model accounts for the existence of undetected species, and variability in abundance and detectability among species. Species-level detection nondetection is linked to species-level abundance via a detection model that accommodates the expectation that probability of detection (at least one individuals is detected) increases with local abundance of the species. We applied this model to a 9-year dataset composed of the detection nondetection of forest birds, at a single post-re site (from 7 to 15 years after re) in a montane area of central Japan. The model allocated undetected species into one of the predened functional groups by assuming a prior distribution on individual group membership. 3. The results suggest that 1520 species were missed in each year, and that species richness of communities and functional groups did not change with post-re forest succession. Overall abundance of birds and abundance of functional groups tended to increase over time, although only in the winter, while decreases in detectabilities were observed in several species. 4. Synthesis and applications. Understanding and prediction of large-scale biodiversity dynamics partly hinge on how we can use data eectively. Our hierarchical model for detection nondetection data estimates abundance in space time at species-, functional group-, and community-levels while accounting for undetected individuals and species. It also permits comparison of multiple communities by many types of abundance-based diversity and similarity measures under imperfect detection. Key-words: data augmentation, detection nondetection data, detectability, functional group, hierarchical Bayesian modelling, monitoring, presence absence data

Introduction
The estimation of abundance is fundamental to ecology (Williams, Nichols & Conroy 2001; Krebs 2009). For example,
*Correspondence author. E-mail: yamaura@for.agr.hokudai.ac.jp Deceased. Present address: Division of Environmental Resources, Graduate School of Agriculture, Hokkaido University, Nishi 9 Kita 9, Kitaku, Sapporo, Hokkaido 060-8589, Japan.

abundance is directly linked to persistence of populations (Hanski 1999) and ecosystem function services (Ellison et al. 2005; Gaston & Fuller 2008). However, large-scale surveys are very costly so abundance can be expensive to count. Binary recording of species (species-level detection nondetection) could reduce sampling eort at each site (MacKenzie et al. 2006), and yet retain some ability to study temporal population dynamics (Joseph et al. 2006; Pollock 2006). Occupancy estimated from binary data is also useful in metapopulation

2010 The Authors. Journal of Applied Ecology 2010 British Ecological Society

68 Y. Yamaura et al. and landscape ecology because theoretical studies use occupancy as a state variable of populations (e.g. Hanski 1999). Collecting binary detection nondetection data is thus increasingly adopted in large-scale eld surveys (Marsh & Trenham 2008). Nevertheless, because of the relevance of abundance in many situations, it is desirable to obtain inferences about abundance from binary data (He & Gaston 2000; Royle & Nichols 2003). Recently, Royle & Nichols (2003) developed a hierarchical model for estimating abundance of single species based on detection nondetection data, i.e. the RoyleNichols (RN) model. In the RN model, species-level detection nondetection is linked to abundance via a detection model that accommodates the expectation that detection probability increases with local abundance of the species. On the contrary, Dorazio & Royle (2005) and Dorazio et al. (2006) developed a multi-species occupancy model also based on species-level detection nondetection data, i.e. the DorazioRoyle (DR) model. By accounting for the existence of undetected species and variability in occupancy and detectability among species, the DR model allows for estimation of species richness and community composition at a given site. Here we developed a novel hierarchical multi-species abundance model by combining these two dierent modelling frameworks, i.e. the RoyleNichols and DorazioRoyle models. Based on species-level detection nondetection data (also called presence absence data), our model provides estimates of abundance of each species within communities while accounting for undetected species and variability in abundance and detectability among species. The concept of a functional group or guild, which is a group of species with similar ecological characteristics, is a basic tool in community ecology (Simberlo & Dayan 1991). It is increasingly important in understanding and predicting how biological communities drive ecosystem function services (Violle et al. 2007; Hillebrand & Matthiessen 2009), and should be incorporated into multi-species abundance models. In our model, we do this by prescribing a prior distribution for species-level group membership in which group identity is a latent categorical covariate. The development of this model made use of 9 years of bird monitoring data from a single site following a forest re. Forest res play a major role in forest ecosystems where they maintain habitat heterogeneity and species diversity at a landscape level (Turner, Gardner & ONeill 2001). They are widely used in conservation management plans (Lindenmayer & Franklin 2002). Although the eect of re on birds has been widely studied, most have used a chronosequence approach (but see Smucker, Hutto & Steele 2005; Haney, Apfelbaum & Burris 2009; Jacquet & Prodon 2009) where bird communities in re and control sites are examined concurrently to identify dierences due to re. However, the assumption of a space-for-time substitution is not necessarily met due to the existence of confounding factors such as dierences in initial conditions and site history among sites (Johnson & Miyanishi 2008). Therefore, long-term monitoring studies examining the eects of re are very valuable (Brawn, Robinson & Thompson 2001). Species detection was recorded over a 9-year period following a major (>200 ha) forest re in Hitachi-city, central Japan (i.e. years 715, post-re). Sampling included both breeding and wintering seasons, allowing comparison of bird responses between two seasons. Long-term monitoring data after forest re are rare especially in East Asia, so these data provide a unique opportunity to understand the responses of birds to such events. The data have only a single spatial replicate (n = 1) but have temporal replications (n = 9 years), and possess two characteristics typical in long-term (or broadspatial) data: variable sampling eort and possible changes in detectability among the samples. These factors complicate estimation of the eects of the covariates on populations and communities because, ideally, sampling should be constant across space and time (i.e. the proportionality assumption: Thompson 2002). We develop a hierarchical model that explicitly incorporates detection processes and accommodates variable sampling eort and changes in detectability, and allows inferences to be made about the post-re changes in bird populations and communities. Several long-term studies from temperate zones (North America: Haney, Apfelbaum & Burris 2009; Europe: Jacquet & Prodon 2009) have shown that bird communities change signicantly in the rst 10 years following a forest re, after which they become relatively stable and approach pre-re communities. Canopy trees return over this period so the abundance of a functional group feeding in the canopy layer (canopy gleaners) is also expected to increase (Haney, Apfelbaum & Burris 2009). However, the species richness and abundance of communities and other functional groups may not change markedly (Haney, Apfelbaum & Burris 2009; Jacquet & Prodon 2009). Succession could cause not only changes in bird communities but also a decline in the detectability of birds due to the development of habitat structure (Bibby & Buckland 1987; Schieck 1997), in which case we predicted that detectability of many species would decline. We tested these predictions by applying our multi-species abundance model to the 9-year monitoring data set.

Materials and methods

THE MODEL

We describe our model using a spatially replicated sampling design as an example, although the model can be easily applied to temporally replicated sampling design by substituting space (e.g. sites) by time (e.g. years). Indeed, we apply this model to temporal dynamics in a bird community in a single site.

Detection process model

We assume a sampling design in which a number of spatial sample units sites are visited multiple times, allowing for inferences to be made about species- and community-level state variables (e.g. occupancy, abundance and species richness) while accounting for imperfect detection (Royle & Dorazio 2008). We utilized binary recording in the eld surveys to obtain encounter histories for each species. This gave a series of detection nondetection in the visitations to each site, e.g. [1 0 1 0 1] for a certain species during ve visits to a site. We compiled these encounter histories into a dataset of the number of visits in

2010 The Authors. Journal of Applied Ecology 2010 British Ecological Society, Journal of Applied Ecology, 48, 6775

Multi-species abundance model 69

which species i are detected (yij) out of total visits (vj) for site j. Here vj needs to be larger than 1, but could vary among sites. A key element of our model is that we link these binary detection nondetection recordings of species to species-level abundance, following Royle & Nichols (2003). If individuals of species i in site j are detected independently of one another with probability rij, then site- and species-specic detection probability is pij 1 1 rij Zij : eqn 1 the community mean response (across species) to a covariate and rb is the standard deviation (among species). In sum, the hyper-parameters are simply the mean and variance for each covariate as measured across species. Using such hierarchical models we can estimate species- and community-level state variables more precisely, especially for rarely detected species (Zipkin, DeWan & Royle 2009; Zipkin et al. 2010), which is often referred to colloquially as borrowing strength, but species-level estimates (random eects) are pulled in (shrunk) ry towards the community-level means (Sauer & Link 2002; Ke 2010). Parameters that describe variation among species i.e. community-level hyperparameters are relatively well-estimated because the model eectively aggregates data from among species (Link 1999; Sauer & Link 2002). On the contrary, the precision of species-level estimates are highly variable depending on the sample sizes and are relatively more inuenced by the hierarchical model structure.

where pij is the net probability of detection of species i, i.e. Pr(at least 1 individual is detected), and Zij is abundance of species i in site j that may be the object of inference either directly or indirectly. We assume that yij follows a binomial distribution in the form yij $ Binomial(vj, pij). Detectability could also dier among sites, depending on site-specic relevant covariates, which can also aect the abundance of each species (Bibby & Buckland 1987; Schieck 1997). In such cases, we must consider the dependency of the detection probability on the co ry 2008): variates (Ke logitrij a0i xj ai eqn 2

BAYESIAN ANALYSIS BY DATA AUGMENTATION

where xj are measured covariates for site j, rij is individual-level detection probability of species i in site j, and a0i (intercept) and ai (slope) are the parameters to be estimated for species i. Because detection processes are modelled separately from ecological (i.e. abundance) processes, changes in abundance would not be con ry 2008). founded with changes in detectability in our model (Ke

Ecological process model

The abundance of species i, Zij, could vary in space depending on covariates in the form Zij $ Poisson (kij) with logkij b0i xj bi eqn 3

where b0i and bi are the parameters to be estimated for species i. Here b0i (intercept) is a random species eect. If there are no covariates, i.e. if the right hand side of eqn 3 has only b0i, the model allows for heterogeneity only in base-line abundance among species. Deviations from such base-line abundance, which depend on covariates of each site, are modelled by xhj bhi (h = 1, 2, , H). Note that variation in abundance might not be fully captured by measured covariates and the Poisson assumption (Royle & Dorazio 2008). To overcome this potential overdispersion, we can include (spatially structured) random site eects into ry et al. the right hand side of the eqn 3 (Royle et al. 2007; Ke 2009). If this model is applied to a temporally replicated design, it can be extended to include dynamic eects, i.e. to incorporate recruitment and mortality rates, which can be approximated by ry et al. 2009; linear or quadratic time trends in this equation (Ke Russell et al. 2009).

MODELLING VARIATIONS IN PARAMETERS AMONG SPECIES

Although parameters of well-detected species could be independently estimated, there are far too many parameters to be precisely estimated for rare species (and some species will not be detected at all). Hence, we add to the model an additional hierarchical layer and assume that parameters (e.g. ai, and bi) are independent normal random eects, ry & Royle each governed by community-level hyper-parameters (Ke 2009). For example, we assume that bi $ Normal(lb, rb2) where lb is

Let N denote the unknown number of distinct species in the sampled community and let n denote the total number of species that are detected through the sampling across sites (i.e. n N). We cannot know how many species are undetected by sampling, i.e. number of undetected species (N n). As such, we prescribe a prior distribution for N and it is estimated along with the other model parameters by Markov chain Monte Carlo (MCMC) using a method based on data augmentation (Royle, Dorazio & Link 2007). As described above, let yi = (yi1, yi2, , ynj) denote a vector of the j site-specic binary observations of species i (number of visits in which species i are detected in site j). We create a supercommunity of species, one that comprises the n detected species and an arbitrarily large, but known, number of undetected species (potential species) for which yi = 0 (i = n + 1, n + 2, , N, N + 1, , M). The supercommunity size M is xed. Formally, data augmentation arises under a uniform prior distribution for the community size N where M is the upper bound for the uniform prior. A useful fact associated with the uniform prior is that it can be constructed hierarchically by introducing a set of latent indicator variables, say wi, which takes the value 1 if a species in the supercommunity is a member of the community exposed to the sampling and 0 otherwise. The uniform prior for N arises by assuming that wi are independent, Bernoulli-distributed random variables indexed by parameter X: wi $ Bernoulli[X]; X $ Uniform(0,1). We P can estimate N as a derived parameter, by calculating M i1 wi . If the assigned value of M is too low, the posterior distribution of X will be concentrated near the upper limit of its support, and N would be underestimated. Conversely, if M is too large, the computational burden increases (Royle & Dorazio 2008). Under data augmentation in our multi-species abundance model, the observations for which wi = 0 are structural or xed 0s. This model admits that the number of visits in which species i is detected (yij) of the species exposed to the sampling (i.e. wi = 1) can be more than 0 depending on covariates, whereas those of the species unexposed to the sampling (i.e. wi = 0) is always 0, that is, Pr(yi = 0) = 1. This is a form of zero-ination model for the augmented data set, and the model is a mixture of stochastic and structural zeros. To formulate this in the model, we modify eqn 1 so that Zijwi rather than Zij appears in the model for encounter probability. We can estimate site-specic species richness and total abundance by P counting species with Zijwi > 0, and calculating M i1 Zij wi , respectively. We calculated the posterior distributions of these derived parameters by MCMC.

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70 Y. Yamaura et al.
We extended the model to include a species-level functional group attribute, as a discrete, latent variable, so that undetected species could be allocated to prescribed functional groups. To formalize this in the model, we introduce a species-level covariate, Gi, the group membership of species i, which is unobserved for the undetected species. We assume that the group membership probabilities have a conventional non-informative Dirichlet prior distribution (Spiegelhalter et al. 2003; McCarthy 2007) on functional group membership. Specically, we assume that Gi $ Categorical(propk) where propk is the proportion of species in group k (k = 1, 2, , K). We used the gamma distribution to construct the Dirichlet prior (Spiegelhalter et al. 2003): gk $  PK Gamma(1,1); propk gk k1 gk . The parameters gk are also estimated by MCMC along with the other parameters of the model. We can estimate species richness of each functional group P by calculating M i1 wi only for members of each group. We can also estimate site-specic species richness and abundance of each functional group by counting members with Zijwi > 0, and calP culating M i1 Zij wi only for the constituent species, respectively.
MODEL APPLICATION

ysis contained 47 and 34 bird species in the wintering and breeding seasons, respectively (Appendix S2). Using the model described above, we estimated temporal dynamics of species richness and abundance within communities and functional groups, and abundance of each species allowing for undetected species. Here we assumed that our data were independent between years because our primary objective was the development and application of the simple model. We augmented the data set with 100 potential species in both seasons. Median estimates of inclusion rate (X) were lower than 1 in both seasons (<045), indicating that the number of augmented species was suciently large (Royle & Dorazio 2008). Because Jacquet & Prodon (2009) showed that bird abundances could change nonlinearly during the 715 post-re years, we modelled abundance response of each species to year since burning (Yearj; covariate) quadratically: logkij b0i b1i Yearj b2i Year2 j: eqn 4

We applied our model to 9-years of bird monitoring data after a forest re at a single site (N36 35 32, E140 37 20) by substituting time (e.g. years) for space (e.g. sites). The monitoring site was located in a montane area in Hitachi-city, Ibaraki prefecture, central Japan. The montane area dominates the western area of the city, whereas industrial and residential area dominates eastern area. The re burnt 218 ha on 78 March 1991. The re was a stand-replacing re because many canopy trees were burned and became snags, and shrubs and forest oor vegetation was burnt out (Appendix S1, Supporting information). The dominant species before the re were planted Japanese cedar Cryptomeria japonica and red pine Pinus densiora, and natural broadleaved species. A single observer (Kouji Kuboi) walked similar routes (c. 35 km) in the area, and recorded species detection from January 1998 to November 2006 (1176 sampling visits; 715 years post-re). Routes were composed of three sections. The second section (c. 600 m) was a single segment, whereas rst and third sections were composed of 23 segments within 500 m each other. Although the observer arbitrarily selected segments in the rst and third sections (and selected routes were not recorded), the total lengths were similar (dierences were <200 m). The three sections of the routes were sub-samples aggregated into single encounter histories in a single route (site) to form species-level encounter histories. That is, a species was recorded as encountered if it was observed on any section of the route. Data were pooled within breeding (MayJuly) and wintering (DecemberFebruary) seasons separately in each year so that the data are composed of total detections out of number of visits for each species in each season (Appendix S2, Supporting information). Stand level covariates such as stand height were not recorded. In each season, we allocated each species exclusively to one of the seven functional groups (or guilds) based on their feeding ecology and habitat associations following published literature (Amano & Yamaura 2007; Yamaura et al. 2009) and expert knowledge. For the wintering season birds were classied as bush user, canopy gleaner, edge species, oor user, open land species, seed eater, and stem prober; in the breeding season we classied birds as air searcher, bush user, canopy gleaner, edge species, ycatcher, open land species, and stem prober. We excluded water birds in both seasons, and in the breeding season we excluded species that did not breed in the study area (i.e. transients) from the analyses. The data set used for the anal-

As succession progresses, the vegetation structure will become more complex and bird detectability will decrease (Bibby & Buckland 1987; Schieck 1997). Therefore, we also assumed that detectability of each species could change quadratically among years: logitrij a0i a1i Yearj a2i Year2 j: eqn 5

Year, which took values 19, was standardized to a mean 0 and a SD of 10. We allocated each of the undetected species into one of the seven functional groups using a categorical distribution with uninformative Dirichlet prior. We used customary vague priors that reect ignorance about the parameter values: X $ Uniform(0,1); lb0 ; lb1 ; lb2 $ Normal(0,1000); la0 ; la1 ; la2 $ Normal(0,1000). We used uniform distribution for the standard deviations (Gelman 2006): rb0 ; rb1 ; rb2 $ Uniform(0,10); ra0 ; ra1 ; ra2 $ Uniform(0,10). We used WinBUGS Ver. 143 (Lunn et al. 2000) and R2WinBUGS R package Ver. 2116 (Sturtz, Ligges & Gelman 2005) to t the model using MCMC. We ran three chains of 88 000 iterations with dierent initial values, discarded the rst 8000 and thinned by 20, which resulted in 12 000 itera^ tions used for inference. Model convergence was assessed with R ^ of all above described values (the GelmanRubin statistic), and R parameters were less than 112, indicating that our model convergence was good (Gelman & Hill 2007).

Results
We recorded 47 and 34 bird species post-re in the wintering and breeding seasons, respectively. The posterior median speP cies richness ( M i1 wi ) was 57 (95% credible interval [CI]: 48 109) and 55 (36127) in each season over the whole nine years. This suggests that c. 10 (95% CI: 162) and 21 (293) species were not detected in each season throughout the survey. Consistent with previous studies (Haney, Apfelbaum & Burris 2009; Jacquet & Prodon 2009), there were no distinct post-re annual changes in estimated species richness of communities or functional groups in both seasons (Fig. 1, Appendix S3, Supporting Information). The estimated species richness of communities suggests that 1520 species were missed in each year. However, the estimated number of missed species varied among functional groups. While most species would have been detected in the bush user functional group in the breeding

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Multi-species abundance model 71

Wintering season
All species
Est. species rich.
120
120

Breeding season
All species
Est. species rich.

100 80 60 40 20 0

100 80 60 40 20 0

28 54 42 46 30 49 35 53 40
8 10 12 14 16

37 27 39 32 24 41 44 14 17
8 10 12 14 16

Year after fire

Year after fire

Bush user
30
30

Bush user
Est. species rich.
25 20 15 10 5 0

Est. species rich.

25 20 15 10 5 0
8 10 12 14 16

10

12

14

16

Year after fire

Year after fire

Canopy gleaner
30
30

Canopy gleaner
Est. species rich.
25 20 15 10 5 0

Est. species rich.

25 20 15 10 5 0
8 10 12 14 16

10

12

14

16

Year after fire

Year after fire

Fig. 1. Estimated annual changes in species richness of bird communities and two functional groups. Left and right columns show the results of wintering and breeding seasons, respectively. Grey lines show observed species richness in each year. Black solid and dotted lines show predicted values of median and 95% credible intervals (CIs), respectively. Numbers above the x axis show the number of visits in each year. Forest re occurred in 1991, which is here treated as year 1. Because upper limits of CI in canopy gleaners in the breeding season had large values (4243), this line was not included in the gure. We did not directly estimate community-level state variables (e.g. species richness abundance of communities functional groups); rather, these are derived parameters that are functions of species-level abundance.

season, 515 species would have been consistently missed in canopy gleaners and edge species in both seasons (see also Appendix S3). In the winter, the abundance of canopy gleaners showed a weak increasing trend, which was consistent with our prediction (Fig. 2, Appendix S3). The abundance of communities (all species) and many functional groups also showed increasing trends. The abundances of constituent species also showed an increasing trend in the winter (e.g. Japanese bush warbler Cettia diphone for bush user; great tit Parus major for canopy gleaner), indicating that changes in their abundance contributed to the increases in the abundance of communities and functional groups (Fig. 3, Appendix S3). In contrast, few annual changes in the abundance of communities and functional groups were observed in the breed-

ing season, and few species showed annual changes in their abundance (Fig. 3, Appendix S3). Annual changes in detectability varied among species. The detectabilities of many species were quite low and unchanged across years, and these species were rarely detected in the survey (Appendices S1 and S3). Brown-eared bulbul Hypsipetes amaurotis was the only species whose detectability increased with years in both seasons (Appendix S3). However, as predicted, the detectability of many well-detected species decreased with year since re, particularly in the later years (Fig. 3, Appendix S3). For example, detection probabilities of the black-faced bunting Emberiza spodocephala, Japanese bush warbler, and the Siberian meadow bunting Emberiza cioides decreased as a function of time in the wintering, breeding, and both seasons, respectively.

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72 Y. Yamaura et al.

Wintering season
All species
1000 1000

Breeding season
All species
Est. abundance
800 600 400 200 0

Est. abundance

800 600 400 200 0 8 10 12 14 16

10

12

14

16

Year after fire

Year after fire

Bush user
200 200

Bush user
Est. abundance

Est. abundance

150 100 50 0 8 10 12 14 16

150 100 50 0 8 10 12 14 16

Year after fire

Year after fire

Canopy gleaner
200 200

Canopy gleaner
Est. abundance

Est. abundance

150 100 50 0 8 10 12 14 16

150 100 50 0 8 10 12 14 16

Year after fire

Year after fire

Fig. 2. Estimated annual changes in abundance of bird communities and two functional groups. Because upper limits of credible interval (CI) in canopy gleaners in the breeding season had large values (>250), this line was not included.

Discussion
It is important to combine ecological and detection processes in statistical models because ignoring imperfect detection (e.g. false absence) could lead not only to underestimation of occupancy abundance (MacKenzie et al. 2006; McCarthy 2007; Royle & Dorazio 2008), but also to a misunderstanding of the eects of covariates (Tyre et al. 2003; Mazerolle, Desrochers & Rochefort 2005) and undesirable management outcomes (Yoccoz, Nichols & Boulinier 2001). Here we develop a method to examine the eects of covariates on population and community structure while accounting for imperfect detection of individuals. We build on earlier development of such models ry & Royle 2008; Russell et al. 2009; Zipkin, (e.g. Ke DeWan & Royle 2009); specically, our model is novel in that it is the rst community-level abundance model based on species-level binary detection nondetection data that accommodates the existence of undetected species (Appendix S4, Supporting Information). Consideration of abun-

dance and undetected species in community models is important because abundance is a fundamental state variable in basic and applied ecology, and undetected species commonly occur in most practical community sampling scenarios. The model also accommodates functional group structure by assuming a prior distribution of functional group membership and estimating the parameters of that distribution. We applied this model to bird monitoring data collected after a forest re. The results suggested that 10 (95% CI: 162) and 21 (293) species remained undetected throughout the survey in the wintering and breeding seasons, respectively, and 1520 species were also missed in each year. Estimates of the number of undetected species throughout the survey were similar to those derived from the regional species pool. Systematic survey of birds in Ibaraki prefecture suggests that 510 and 2129 undetected species could inhabit the area in each season (Ibaraki Branch 2008; S. I. person. comm.). This suggests that our abundance model may yield good inferences about the sampled community. The estimated number of undetected

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Multi-species abundance model 73

Wintering season
Japanese bush warbler

Breeding season
Japanese bush warbler
10 20 10 08 06 10 5 0 8 10 12 14 16 04 02 00

Est. detectability

20

Est. abundance

15 10 5 0 8 10 12 14 16

08 06 04 02 00

Est. abundance

15

Year after fires

Great tit
10 20

Year after fires

Great tit
10 08 06 10 5 0 8 10 12 14 16 04 02 00

Est. abundance

08 06 04 02 00 8 10 12 14 16

Est. abundance

15 10 5 0

15

Year after fires

Siberian meadow bunting
10 20

Year after fires

Siberian meadow bunting
10 08 06 10 5 0 8 10 12 14 16 04 02 00

Est. detectability

Est. abundance

20 15 10 5 0 8 10 12 14 16

08 06 04 02 00

Est. abundance

15

Year after fires

Year after fires

Fig. 3. Estimated annual changes in abundance of three bird species. Japanese bush warbler, great tit, and Siberian meadow bunting were representative species of bush user, canopy gleaner, and edge species, respectively. Black lines show predicted abundances indexed by left-side ordinate. Thin grey lines shows expected abundances (kij) obtained by eqn 4 and median estimated parameters (bi0, bi1, and bi2). Thick grey lines show expected individual-level detectabilities (rij) obtained by eqn 5 and median estimated parameters (ai0, ai1, and ai2) indexed by right-side ordinate. Dierences in predicted and expected values are due to the fact that predicted values represent a compromise between expected values and observations, which were not strictly consistent with the quadratic models.

species diered among functional groups. We found few annual changes in the estimated species richness of communities and functional groups in both seasons, which is consistent with previous studies (Haney, Apfelbaum & Burris 2009; Jacquet & Prodon 2009). As predicted, the abundance of canopy gleaners showed a trend towards a slight increase across years. The abundance of communities, many functional groups and species also showed consistent increasing trends, but only in the wintering season. Foraging resources, including those in canopy layers, would have increased as succession progressed. In contrast, we found few annual changes in species abundances during the breeding season. Under conditions of severe weather and limited food resources, habitat and landscape structure in winter could have large eects on bird populations and communities (e.g. Doherty & Grubb 2002; Johnson et al. 2006) with further eects in the subsequent breeding season (Greenberg & Marra 2005). Birdhabitat relationships in post-re sites may also be important in winter. Previous studies have shown that bird communities are relatively stable after the rst 10 years post-re in the United

States and Europe (Haney, Apfelbaum & Burris 2009; Jacquet & Prodon 2009). Although we found that bird responses to the year since burning diered between seasons, our study in East Asia conrmed this by accounting for detectabilities over this period. The rst 510 years after a forest re are the most dynamic, during which open-land species (granivores), ycatchers, and woodpeckers colonize, and some of them desert the site (Brawn, Robinson & Thompson 2001; Jacquet & Prodon 2009). It is thought that disturbed early successional habitats and the species inhabiting them are now declining in many countries (Askins 2001; Yamaura et al. 2009), therefore future studies should examine the responses of birds to such short-lived disturbed habitats at multiple scales, preferably using complementary chronosequence and long-term (revisiting) approaches (e.g. Donner, Ribic & Probst 2010). In our model, we assumed the unit of detection was a single individual of a species (Zij = number of individuals). However, many bird species form ocks in winter, for which the observers detect groups of birds rather than single individuals (Zij = number of functional individuals). When estimating abundance of communities and or comparing abundance

2010 The Authors. Journal of Applied Ecology 2010 British Ecological Society, Journal of Applied Ecology, 48, 6775

Est. detectability

Est. detectability

20

Est. detectability

Est. detectability

74 Y. Yamaura et al. among species, group size should be considered whenever possible. However, obtaining explicit information about group size entails additional sampling protocol modications and also additional model assumptions. The development of methods that can accommodate group size would be worthwhile. Rarely detected species had low detectabilities, and the credible intervals (CIs) of community-level state variables (i.e. species richness and abundance of communities and functional groups) were very wide. These results are attributable to the low densities of many species in the community, factors that cause low detectability (e.g. topographic complexity along the census route, poor census ability of the observer), short length of the census route, and the limited amount of information provided by binary detection nondetection data. In addition, our model is highly parameterized relative to the sparse data available; however, this is partly a consequence of biological considerations. In order to accommodate temporal variability in the parameters in the model, it is necessary to consider heterogeneity in model parameters among species. In our case, we considered a quadratic trend containing species-level linear and quadratic parameters. For many species, these specieslevel parameters are poorly informed by the sparseness of available data. Indeed, narrower CIs could have been achieved if we assumed constant detectability across years, i.e. by using ri rather than rij (results not shown). Such a model might be reasonable in a standard design where spatial units with similar habitat structure are used as replicates, and sampled within the same year. However, in our case, such a model could not account for the decreases in detectabilities in the later years, and estimated bird abundances showed slight decreases in that period especially in the winter. If we use count data rather than binary detection nondetection, sparse data availability would be partially resolved. For example, in each site, we may obtain count data such as counts of individuals in the series of the vis ry, Royle & Schmid 2005). Let yijt (t = 1, its, e.g. [2 1 3 0 2] (Ke 2, , T) be independent counts of individuals of species i made at sites j = 1, 2, , J so that yijt $ BinomialZij ; rij eqn 6 ness could be dened as a diversity (local diversity). Dierences between these two diversity measures could be an estimate of b diversity (among sites diversity). Collection of detection nondetection data for species is increasingly adopted in large-scale eld surveys. Development, use, and improvement of the statistical models for such simple data should be encouraged. Our hierarchical multi-species model allows explicit modelling and estimation of abundance in space time at species-, functional group- and communitylevels accounting for undetected individuals and species.

Acknowledgements
Suggestions from two anonymous reviewers and the editor greatly improved ry, R. Russell, and E. F. Zipkin for our manuscript. We are grateful to M. Ke their helpful reviews of a draft of this manuscript. We also thanks for T. Amano, K. Matsumoto, Y. Mitsuda, H. Taki, K. Okabe, and S. Sugiura for useful suggestions for this study. Y. Yamaura was supported by Research grant No. 200802 of the Forestry and Forest Products Research Institute, and JSPS KAKENHI (Grand-in-Aid for JSPS Fellows No. 21-7033).

References
Amano, T. & Yamaura, Y. (2007) Ecological and life-history traits related to range contractions among breeding birds in Japan. Biological Conservation, 137, 271282. Askins, R.A. (2001) Sustaining biological diversity in early successional communities: the challenge of managing unpopular habitats. Wildlife Society Bulletin, 29, 407412. Bibby, C.J. & Buckland, S.T. (1987) Bias of bird census results due to detectability varying with habitat. Acta Oecologica, 8, 103112. Brawn, J.D., Robinson, S.K. & Thompson, F.R. III. (2001) The role of disturbance in the ecology and conservation of birds. Annual Review of Ecology and Systematics, 32, 251276. Doherty, P.F.J. & Grubb, T.C.J. (2002) Survivorship of permanent-resident birds in a fragmented forested landscape. Ecology, 83, 844857. Donner, D.M., Ribic, C.A. & Probst, J.R. (2010) Patch dynamics and the timing of colonization-abandonment events by male Kirtlands Warblers in an early succession habitat. Biological Conservation, 143, 11591167. Dorazio, R.M. & Royle, J.A. (2005) Estimating size and composition of biological communities by modeling the occurrence of species. Journal of the American Statistical Association, 100, 389398. Dorazio, R.M., Royle, J.A., So derstro m, B. & Glimska r, A. (2006) Estimating species richness and accumulation by modeling species occurrence and detectability. Ecology, 87, 842854. Ellison, A.M., Bank, M.S., Clinton, B.D., Colburn, E.A., Elliott, K., Fort, C.R. & Foster, D.R. (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and Environment, 3, 479486. Gaston, K.J. & Fuller, R.A. (2008) Commonness, population depletion and conservation biology. Trends in Ecology and Evolution, 23, 1419. Gelman, A. (2006) Prior distributions for variance parameters in hierarchical models. Bayesian Analysis, 1, 513534. Gelman, A. & Hill, J. (2007) Data Analysis Using Regression and Multilevel hierarchical Models. Cambridge University Press, Cambridge. Greenberg, R. & Marra, P.P. (2005) Birds of Two Worlds: The Ecology and Evolution of Migration. Johns Hopkins University Press, Baltimore. Haney, A., Apfelbaum, S. & Burris, J.M. (2009) Thirty years of post-re succession in a southern boreal forest bird community. American Midland Naturalist, 159, 421433. Hanski, I. (1999) Metapopulation Ecology. Oxford University Press, Oxford. He, F. & Gaston, K.J. (2000) Estimating species abundance from occurrence. American Naturalist, 156, 553559. Hillebrand, H. & Matthiessen, B. (2009) Biodiversity in a complex world: consolidation and progress in functional biodiversity resarch. Ecology Letters, 12, 14051419. Ibaraki Branch (2008) Report on the Distribution of Wild Birds and Mammals in Ibaraki Prefecture (2006, 2007). Ibaraki Branch, Wild Bird Society of Japan, Mito.

where Zij and rij is abundance and individual-level detectability of species i in site j, respectively. Development of multi-species models for this binomial observation model is ongoing.

Conclusion
Because our model estimates the abundance of each species, we can compare multiple communities by many types of abundance-based diversity and similarity measures under imperfect detection (e.g. Shannon diversity index, Euclidean distance and v2 metric: Legendre & Legendre 1998). A further extension is the estimation of a, b, and c diversity. Using the additive partitioning framework (Lande 1996; Veech et al. 2002), the estimated species richness of the sampled community (N) could be dened as c diversity (regional diversity), while average site-specic species rich-

2010 The Authors. Journal of Applied Ecology 2010 British Ecological Society, Journal of Applied Ecology, 48, 6775

Multi-species abundance model 75

Jacquet, K. & Prodon, R. (2009) Measuring the postre resilience of a birdvegetation system: a 28-year study in a Mediterranean oak woodland. Oecologia, 161, 801811. Johnson, E.A. & Miyanishi, K. (2008) Testing the assumptions of chronosequences in succession. Ecology Letters, 11, 419431. Johnson, M.D., Sherry, T.W., Holmes, R.T. & Marra, P.P. (2006) Assessing habitat quality for a migratory songbird wintering in natural and agricultural habitats. Conservation Biology, 20, 14331444. Joseph, L.N., Field, S.A., Wilcox, C. & Possingham, H.P. (2006) Presenceabsence versus abundance data for monitoring threatened species. Conservation Biology, 20, 16791687. ry, M. (2008) Estimating abundance from bird counts: binomial mixture Ke models uncover complex covariate relationships. Auk, 125, 336345. ry, M. (2010) Introduction to WinBUGS for Ecologists: A Bayesian Approach Ke to Regression, ANOVA, Mixed Models and Related Analysis. Academic Press, San Diego. ry, M. & Royle, J.A. (2008) Hierarchical Bayes estimation of species richness Ke and occupancy in spatially replicated surveys. Journal of Applied Ecology, 45, 589598. ry, M. & Royle, J.A. (2009) Inference about species richness and community Ke structure using species-specic occupancy models in the national Swiss breeding bird survey MHB. Modeling Demographic Processes in Marked Populations (eds D.L. Thomson, E.G. Cooch & M.J. Conroy), pp. 639656. Springer, New York. ry, M., Royle, J.A. & Schmid, H. (2005) Modeling avian abundance from Ke replicated counts using binomial mixture models. Ecological Applications, 15, 14501461. ry, M., Dorazio, R.M., Soldaat, L., van Strien, A., Zuiderwijk, A. & Royle, Ke J.A. (2009) Trend estimation in populations with imperfect detection. Journal of Applied Ecology, 46, 11631172. Krebs, C.J. (2009) Ecology: The Experimental Analysis of Distribution and Abundance. Pearson Education, Chollerstrasse. Lande, R. (1996) Statistics and partitioning of species diversity, and similarity among multiple communities. Oikos, 76, 513. Legendre, P. & Legendre, L. (1998) Numerical Ecology, 2nd edn. Elsevier, Amsterdam. Lindenmayer, D.B. & Franklin, J.F. (2002) Conserving Forest Biodiversity: A Comprehensive Multiscaled Approach. Island Press, Washington, DC. Link, W.A. (1999) Modeling pattern in collections of parameters. Journal of Wildlife Management, 63, 10171027. Lunn, D.J., Thomas, A., Best, N. & Spiegelhalter, D. (2000) WinBUGS a Bayesian modelling framework: concepts, structure, and extensibility. Statistics and Computing, 10, 325337. MacKenzie, D.I., Nichols, J.D., Royle, J.A., Pollock, K.H., Bailey, L.L. & Hines, J.E. (2006) Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence. Academic Press, Amsterdam. Marsh, D.M. & Trenham, P.C. (2008) Current trends in plant and animal population monitoring. Conservation Biology, 22, 647655. Mazerolle, M.J., Desrochers, A. & Rochefort, L. (2005) Landscape characteristics inuence pond occupancy by frogs after accounting for detectability. Ecological Applications, 15, 824834. McCarthy, M.A. (2007) Bayesian Methods for Ecology. Cambridge University Press, Cambridge. Pollock, J.F. (2006) Detecting population declines over large areas with presence-absence, time-to-encounter, and count survey methods. Conservation Biology, 20, 882892. Royle, J.A. & Dorazio, R.M. (2008) Hierarchical Modeling and Inference in Ecology: The Analysis of Data From Populations, Metapopulations and Communities. Academic Press, Amsterdam. Royle, J.A., Dorazio, R.M. & Link, W.A. (2007) Analysis of multinomial models with unknown index using data augmentation. Journal of Computational and Graphical Statistics, 16, 6785. Royle, J.A. & Nichols, J.D. (2003) Estimating abundance from repeated presence-absence data or point counts. Ecology, 84, 777790. ry, M., Gautier, R. & Schmid, H. (2007) Hierarchical spatial Royle, J.A., Ke models of abundance and occurrence from imperfect survey data. Ecological Monographs, 77, 465481. Russell, R.E., Royle, J.A., Saab, V.A., Lehmkuhl, J.F., Block, W.M. & Sauer, J.R. (2009) Modeling the eects of environmental disturbance on wildlife communities: avian responses to prescribed re. Ecological Applications, 19, 12531263. Sauer, J.R. & Link, W.A. (2002) Hierarchical modeling of population stability and species group attributes from survey data. Ecology, 86, 17431751. Schieck, J. (1997) Biased detection of bird vocalizations aects comparisons of bird abundance among forested habitats. Condor, 99, 179190. Simberlo, D. & Dayan, T. (1991) The guild concept and the structure of ecological communities. Annual Review of Ecology and Systematics, 22, 115 143. Smucker, K.M., Hutto, R.L. & Steele, B.M. (2005) Changes in bird abundance after wildre: importance of re severity and time since re. Ecological Applications, 15, 15351549. Spiegelhalter, D., Thomas, A., Best, N. & Lunn, D. (2003) WinBUGS User Manual. Ver. 1.4. MRC Biostatistics Unit, Institute of Public Health, Cambridge. Sturtz, S., Ligges, U. & Gelman, A. (2005) R2WinBUGS: a package for running WinBUGS from R. Journal of Statistical Software, 12, 116. Thompson, W.L. (2002) Towards reliable bird surveys: accounting for individuals present but not detected. Auk, 119, 1825. Turner, M.G., Gardner, R.H. & ONeill, R.V. (2001) Landscape Ecology in Theory and Practice: Pattern and Process. Springer, New York. Tyre, A.J., Tenhumberg, B., Field, S.A., Niejalke, D., Parris, K. & Possingham, H.P. (2003) Improving precision and reducing bias in biological surveys: estimating false-negative error rates. Ecological Applications, 13, 17901801. Veech, J.A., Summerville, K.S., Crist, T.O. & Gering, J.C. (2002) The additive partitioning of species diversity: recent revival of an old idea. Oikos, 99, 39. Violle, C., Navas, M.-L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I. & Garnier, E. (2007) Let the concept of trait be functional! Oikos, 116, 882 892. Williams, B.K., Nichols, J.D. & Conroy, M.J. (2001) Analysis and Management of Animal Populations. Academic Press, San Diego. Yamaura, Y., Amano, T., Koizumi, T., Mitsuda, Y., Taki, H. & Okabe, K. (2009) Does land-use change aect biodiversity dynamics at a macroecological scale? A case study of birds over the past 20 years in Japan. Animal Conservation, 12, 110119. Yoccoz, N.G., Nichols, J.D. & Boulinier, T. (2001) Monitoring of biological diversity in space and time. Trends in Ecology and Evolution, 16, 446453. Zipkin, E.F., DeWan, A. & Royle, J.A. (2009) Impacts of forest fragmentation on species richness: a hierarchical approach to community modelling. Journal of Applied Ecology, 46, 815822. Zipkin, E.F., Royle, J.A., Dawson, D.K. & Bates, S. (2010) Multi-species occurrence models to evaluate the eects of conservation and management actions. Biological Conservation, 143, 479484. Received 5 June 2010; accepted 10 November 2010 Handling Editor: Marc Cadotte

Supporting information
Additional Supporting Information may be found in the online version of this article. Appendix S1. Some pictures of the study area. Appendix S2. Encounter histories of forest birds and guild classication. Appendix S3. Annual changes in birds. Appendix S4. Model categorization by inference targets and state variables. Appendix S5. R code and required data les to conduct our multi-species abundance model. As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing les) should be addressed to the authors.

2010 The Authors. Journal of Applied Ecology 2010 British Ecological Society, Journal of Applied Ecology, 48, 6775