We asked whether these impacts of humans on regional seabird populations may also have contributed indirectly to long-term change in plant communities on Mandarte Island. To do so, we used opportunistic and systematic data sets collected over 116 years (non-continuously), including historical photographs, expedition notes, published accounts, and historical and contemporary surveys of plant species cover, richness and soil nutrients to ask: (1) how native and exotic plant species richness and cover changed on Mandarte Island from 1896 to 2012; and (2) what contemporary relationships exist between gull presence and plant community composition on islands in our study region with and without gull breeding colonies. Our results support the suggestion that humans affect plant communities indirectly via their effects on seabird abundance ( Croll et al., 2005 ) and imply that population increases in gulls over the last century have facilitated rapid change in plant communities on islands with nesting seabirds.

Vegetation survey data from Mandarte Island collected in paired plots in 1986 and 2006 were compared using Wilcoxon matched-pairs tests. For comparisons of quadrat data on gull and non-gull islands we used Wilcoxon signed-rank tests to test for differences in native and exotic species richness and cover and total soil N and C. To test for links between native and exotic species richness, cover, and soil conditions on gull versus non-gull islands we used generalized linear mixed models. Specifically, we constructed models to explain cover and richness, native cover and richness, and the proportion of exotic vs. native cover and richness using soil depth, total soil N and C, and presence of seabirds as fixed effects. We included island identity as a random factor in these models to account for repeat sampling within islands. Percentage cover was transformed using arcsine square root (for proportion) and richness was transformed using log+1 to normalize residual errors. We selected models based on AIC and estimated p-values for predictors using Markov-chain Monte Carlo sampling ( Baayen, Davidson & Bates, 2008 ). Total N and C were highly correlated; however, because exploratory models indicated that each variable explained an independent fraction of variation in plant survey data, both variables were retained in our analyses, but interpreted cautiously. All mixed models used the lme4 package ( Bates, Maechler & Bolker, 2012 ) in R v.2.15.1 ( R Development Core Team, 2014 ).

In June 2012, we also conducted contemporary surveys on islands adjacent to Mandarte Island to compare native species richness and cover, exotic species richness and cover, and total N and C in soil on islands with and without nesting glaucous-winged gulls, including three islands with gull colonies (‘gull islands’), namely Mandarte, Arbutus (48.71 N, −123.44 W, 35–150 nesting pairs, 1976–2010) and the unnamed islet south of Mandarte (48.63 N, −123.28 W, 0–106 nesting pairs, 1962–2010; Drent et al., 1964 ; Blight, 2012 ). Cover of herbaceous and grass species and bare soil were estimated following Bennett et al. (2012 ; N = 14 × 1 m 2 quadrats on Mandarte Island; N = 4 on Arbutus Island; N = 3 on unnamed islet). Quadrat locations were selected randomly within grid cells, for a random set of all mapped grid-squares that included meadow habitat. Plot-level data on soil depth was collated as the mean of four depths at quadrat corners. Total soil nitrogen, carbon and moisture were estimated by collecting 100 g of soil from five sub-samples ca. 2 cm below the rooting zone, then sieved (2 mm) and ground (≤ 0.14 mm) for analysis (Fisons NA-1500 combustion elemental analyser). Soil moisture was estimated from oven-dried (105 °C) sub-samples. Data from 21 quadrats collected on the three gull islands were compared to 57 quadrats from 22 islands in the same region not known to have supported persisting gull populations (‘non-gull islands’; Table S2 ).

To estimate temporal change in shrub species richness and cover on Mandarte Island, we surveyed vegetation cover from June–July, 1986 and 2006, in 132, 20 × 20 m grid-squares mapped onto a 1974 air photo. Surveys comprised c 90% of island area, but excluded some areas at the edge of sparsely- or non-vegetated bluffs. In each square we estimated the percent cover of all perennial shrubs and common herbaceous plants by species, exposed rock, and all graminoids as a group. Soil depth was estimated by hammering a graduated rod into the soil at five equidistant locations at the square and 1 m in from each corner of the square.

Partial accounts of Mandarte Island flora and fauna appear as museum records as early as 1896, including notes on seabird presence and abundance, plant species occurrence, and photographs, all depicting a vegetation community historically characteristic of a maritime Garry oak ecosystem (e.g., Tompa, 1963 ; Drent et al., 1964 ). Various researchers subsequently conducted periodic surveys after 1955, mainly recording plants as species lists and seabirds as counts, but also documenting early changes in the plant community and linking those changes to contemporary increases in gull and cormorant numbers ( Drent et al., 1964 ). We compiled historical records of plant species occurrence from the archived museum reports, herbarium specimens and lists provided by Tompa (1963) and Drent et al. (1964) , and then compared these lists to contemporary surveys conducted by P.A., M.G. and T.K.L. Here, we list all plant species recorded on Mandarte Island to 2012 and classified each as extirpated or extant, and as native or exotic to the Pacific coast of North America ( Table S1 ). Historical photos of the island also allow qualitative comparisons to a 1963 photo by P. Grant covering a sizeable portion of Mandarte Island and including all typical habitats, which we replicated in 2002 ( Fig. 1 ).

The presence of gull colonies was the only fixed effect retained in generalized mixed models to predict exotic cover (positive effect), the proportion of exotic versus native cover (positive effect), and native richness (negative effect; Table 1 ). In contrast, total C was the only fixed effect retained in models predicting exotic richness (negative effect) and native cover (positive effect). Both total C and total N were retained in the top model to predict proportion exotic and native species richness, whereas soil depth was not retained in any top model ( Table 1 ).

Quadrats on gull islands also yielded higher total nitrogen (N) and total carbon (C) concentrations than on non-gull islands (nitrogen: 2.86 ± 0.17% with vs. 1.66 ± 0.10% without; p < 0.001; carbon: 30.31 ± 2.03% with vs. 23.19 ± 1.44% without; p = 0.01). Total C and N were also positively related to soil depth ( r = 0.58, p = 0.006 and r = 0.51, p = 0.02; respectively), but only on gull-islands. In contrast, mean soil depth was similar on gull and non-gull islands (11.14 ± 1.33 with vs. 19.37 ± 2.51 cm).

Comparisons of contemporary surveys in 1986 and 2006 indicate a 31% decline in shrub cover on Mandarte Island (N = 132, p = 0.002). On average, snowberry ( Symphoricarpos albus ) declined from 33 to 19% cover (p < 0.001), Nootka rose ( Rosa nutkana ) from 24 to 20% (p = 0.04), and gooseberry ( Ribes divericatum ), from 3 to 0.8% (p < 0.001), whereas the exotic Himalayan blackberry ( Rubus armeniacus ) and native red elderberry ( Sambucus racemosa ) increased from 2 to 18% and 1 to 6%, respectively (p < 0.001). The extent of bare rock declined from 38 to 34% (p = 0.03) as grass cover increased (31 to 40%; p < 0.001).

Over 116 years we detected 18 extirpations of native species from Mandarte Island, representing a loss of 32% of all native plant species recorded there. In contrast, we detected 31 colonization events by exotic species, two apparent colonisations of native species, and four extirpations of exotic species known to have become established prior to 1960 ( Table S1 ). Forty-five native and one exotic species identified on Mandarte Island prior to 1960 remained extant on the island as of 2012, but 94% of exotic colonization events occurred after 1960. Visual comparison of historic and contemporary photos ( Fig. 1 ) and our observations over 35 years (PA) also suggest long-term declines in shrub cover and extent of bare rock. Photos document the extirpation of three tree species: grand fir ( Abies grandis ), arbutus ( Arbutus menziesii ) and Douglas-fir ( Pseudotsuga menziesii ). Comparing the diameter of dead Douglas-fir on Mandarte (c 60–180 cm DBH) to felled trees of similar size on adjacent islands suggests the largest individuals on Mandarte Island recruited about 300 yrs BP (P. Arcese, 2016, unpublished data).

Discussion

A comparison of historical and modern vegetation surveys confirms that substantial change in plant species cover, richness and origin occurred from 1896–2012 on Mandarte Island. Observations from historic photographs, plant lists and anecdotal reports are also consistent with the idea that these changes were driven in part by increases in the abundance of nesting seabirds on the island after 1920. Contemporary surveys of 24 islands with and without nesting seabirds further suggested that nesting seabirds increase soil C, N and depth, which can facilitate non-native grasses and inhibit recruitment and survival in native plant species adapted to poor, shallow soils (e.g., Bennett et al., 2012; Best & Arcese, 2009). Gulls and other surface-nesting seabirds such as cormorants are also reported as agents of change in soil and plant communities elsewhere (Ellis, 2005; Mulder et al., 2011). Thus, despite limits on the quality and scope of our data, our results are consistent with the idea that long-term vegetation change on Mandarte Island has been caused in part via the effects of humans on seabird abundance.

Direct impacts of seabirds on vegetation include the input and distribution of guano, which can be toxic or inhibit photosynthesis (Ishida, 1997), and physical disturbance due to trampling, nest construction and territory defence (Sobey & Kenworthy, 1979; Ellis, 2005). As reported elsewhere, we also found that islands with gull colonies had higher soil C and N concentrations than those without them (e.g., Anderson & Polis, 1999; Wait, Aubrey & Anderson, 2005). Ellis (2005) suggested that surface-nesting seabirds enhanced soil depth in systems without mammalian herbivores by facilitating litter accumulation; this observation is consistent with an observed decline in exposed rock on Mandarte Island, and with positive correlations between soil depth and C and N concentrations on islands with (but not without) gull colonies. In addition to the effects of seabirds, however, we also acknowledge that many other changes have occurred in our study system over the last century, including changes in the use of fire to maintain communities’ aboriginal peoples of the region (Macdougall & Turkington, 2005, Arcese et al., 2014), as well as increased visitation by European colonists and others. While it is possible that the cessation of burning might increase soil depth over time, burning also ceased on a number of the islands without nesting seabirds, which still support most or all of the plant species extirpated from Mandarte Island (Bennett & Arcese, 2013). We are also unaware of any systematic differences between the islands we surveyed with and without gulls linked to their size, isolation or human visitation rates that could account for the floristic differences we report.