Evidence of Seabird Guano Enrichment on a Coral Reef in Oahu, Hawaii

Mar Biol (2016) 163:22 DOI 10.1007/s00227-015-2808-4

ORIGINAL PAPER

Evidence of seabird guano enrichment on a coral reef in Oahu, Hawaii

Susanna E. Honig1,2 · Brenna Mahoney1

Received: 10 August 2015 / Accepted: 20 December 2015 © Springer-Verlag Berlin Heidelberg 2016

Abstract Seabirds and coral reefs are two of the most Introduction threatened marine communities on earth, and they co-occur on many tropical islands and subtropical islands and atolls. Seabirds typically forage at sea but breed and roost, some- Seabirds concentrate marine-derived nutrients on breeding times in large numbers, on islands where they deposit islands in the form of feces (guano), and these nutrients nitrogen- and phosphorus-rich guano. Guano is docu- dramatically alter terrestrial ecosystem ecology. Recent mented to provide a significant nutrient input in terrestrial work in the remote Pacific indicates seabird-derived nutri- (e.g., Polis and Hurd 1996; Croll et al. 2005; Young et al. ents may also subsidize nearshore coral reefs, but the con- 2010) and marine (Wootton 1991; Kolb et al. 2010) eco- sequences of guano on complex, anthropogenically modi- systems, increasing primary production with the potential fied coral reefs are unknown. The impact of seabird guano to fuel production at higher trophic levels (McCauley et al. on nearshore coral reefs around Moku Nui, an islet with a 2012). Coral reefs are often found adjacent to islands with large seabird colony in Oahu, Hawaii, was investigated in large populations of breeding or roosting seabirds, pro- comparison with coral reefs around three islets with lower viding the opportunity for nutrients derived from seabird seabird abundance. Reefs in close proximity to Moku Nui guano deposited on the islands to be transported to the (where thousands of wedge-tailed shearwaters, Puffinus adjacent coral reef ecosystems. Many coral reefs are also pacificus, breed) had greater concentrations of dissolved far from pristine and are instead subject to local stressors phosphate in seawater and greater δ15N in adjacent subtidal such as overfishing (Pandolfi et al. 2003), nutrient pollu- macroalgae relative to reefs next to smaller breeding colo- tion (Fabricius 2005), and habitat transformation (Nystrom nies. However, dissolved nitrate was not different among et al. 2000) as well as global stressors including ocean islets. These results indicate that seabirds may be a source acidification, sea level rise, and increasing water tempera- of nutrients for the waters surrounding Moku Nui that are ture (Hoegh-Guldberg et al. 2007). Nutrient pollution from already inundated with local and global stressors. anthropogenic sewage (e.g., Lapointe and Clarke 1992) or agricultural fertilizer (e.g., Fabricius and De’Ath 2004) can harm recipient scleractinian corals directly via reduced growth rates stemming from competition with endosymbi- Responsible Editor: V. Paiva. onts and indirectly via increased sedimentation, reduced Reviewed by F.C. Ceia and an undisclosed expert. light, and competition with weedy algal species that flour- ish in the presence of excess nutrients (reviewed in Fab- * Susanna E. Honig ricius 2005). Furthermore, on reefs that are heavily fished, [email protected] excess nutrients can contribute to phase shifts that trans- 1 Ecology and Evolutionary Biology Department, University form high biodiversity, coral-dominated reefs into lower of California Santa Cruz, Santa Cruz, CA 95064, USA diversity algal-dominated habitats (e.g., Hughes 1994). It 2 Molecular, Cell and Developmental Biology Department, is therefore unclear how naturally derived nutrients from University of California Santa Cruz, Santa Cruz, CA 95064, seabird colonies will affect coral reefs experiencing mul- USA tiple stressors.

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Coral reefs in the main Hawaiian Islands have been have more dissolved nutrients and that sampled macroal- exposed to numerous anthropogenic stressors for centu- gae will have higher δ15N values, a proxy for seabird- ries, the most extreme of which occur on Oahu, the most derived nitrogen, compared to islets with fewer seabirds. populated island with almost 1 million inhabitants (Bai- ley-Brock et al. 2007). Oahu’s coral reefs have undergone significant modification stemming from agricultural devel- Materials and methods opment, land use change, effluent from human sewage, invasive species, and intensive fishing (Hunter and Evans Study site 1995). Many of these threats are concentrated on reefs adjacent to Honolulu, the island’s urban center, but reefs We carried out our study during February through March around the entire island are also subject to various levels of 2012 on four small islets, Mokoli’i, Kapapa, Popoi’a, and anthropogenic stressors. Moku Nui, which are offshore of windward Oahu (Fig. 1). Many of Oahu’s coral reefs are adjacent to small off- Moku Nui, Popoi’a, and Kapapa are all uninhabited seabird shore islets where seabirds breed. Oahu’s offshore islets sanctuaries managed by the Hawaii Department of Land are partially isolated from many of the anthropogenic and Natural Resources Division of Forestry and Wildlife disturbances in comparison with the main island of Oahu (DLNR DOFAW), while Mokoli’i is under city jurisdic- and are thus the breeding site for approximately 98 % of tion and part of Kualoa Regional Park. Together, Moku the 145,000 seabirds breeding in the Oahu region (Pyle Nui and its southern neighbor Moku Iki form the Mokuluas and Pyle 2009). These islets are uninhabited with vary- which host more than 10,000 breeding seabirds per year ing accessibility to humans and therefore represent an (Table 1, Pyle and Pyle 2009), making Moku Nui the islet intermediate level of disturbance when compared to the with the highest seabird abundance in our study by over highly disturbed main Hawaiian Islands and protected sixfold. The dominant species breeding across these islets northwestern Hawaiian Islands (Coles and Swenson are wedge-tailed shearwaters Puffinus pacificus, but other 2010). Differences in proximity, protection status, inva- species found breeding on one or all of these islets include sive species, and size have resulted in a large gradient Bulwer’s petrels Bulweria bulwerii, Christmas shearwaters in seabird abundance among islets, providing a unique Puffinus nativitatis, and white-tailed tropicbirds Phaethon opportunity to investigate the influence of relative sea- lepturus (Pyle and Pyle 2009). We visited these sites in the bird abundance among islets on nearshore seawater and middle of the rainy season, which is November through algal biogeochemistry. In this study, we use an island/ April (Timm et al. 2015), with the assumption that nutri- reef pair with thousands of breeding seabirds (Table 1) ents concentrated on islands in the past breeding season and compare it to three island/reef pairs with signifi- (June–August, Pyle and Pyle 2009) may be mobilized dur- cantly smaller seabird populations (Table 1), to assess ing the wet season (e.g., Smith and Johnson 1995). whether differences in seabird abundance are associated with differences in dissolved nutrients (phosphate and Seawater nutrients nitrate) and macroalgal δ15N. We hypothesize that coral reef waters next to more abundant seabird colonies will On the leeward side of each islet, we collected three mid- water column seawater samples (~3–5 m above depth, which varied) at 6 sites (separated by 8 m) adjacent to the Table 1 Characteristics of Mokoli’i, Kapapa, Popoi’a, and Mokuluas islet (n 72 total samples, 18 per islet) in 500-mL acid- islets = washed HDPE bottles. Samples were collected within Islet Latitude Longitude Number of Number of a range of 45–90 m from the shoreline of each islet. We breeding breeding stored bottles on ice and filtered each sample through seabirdsa seabirds along linear coastline Whatman GF/F 25-mm filters using hand-pump vacuum 1 b (# m− ) filtration systems upon our return to the Hawaii Institute of Marine Biology. We froze filtrate in 20-mL scintillation Mokoli’i 21.51 157.83 202 0.27 − vials and shipped them on dry ice to the Marine Analytical Kapapa 21.48 157.80 310 0.30 − Laboratory at the University of California Santa Cruz. We Popoi’a 21.40 157.72 1625 2.39 − then analyzed thawed seawater with a Lachat QuikChem Mokuluas 21.39 157.69 10,155 6.80 − 8000 Flow Injection Analyzer to measure dissolved NOx 3 a Estimate from Pyle and Pyle (2009) (nitrate nitrite) and PO − (phosphate) levels (μM). + 4 b Linear coastline measured with path tool in Google Earth (Google Manufacturer method detection limits (MDL) were set at 3 Inc. 2015) 0.02 μM for PO4 − and 0.01 μM for NOx.

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Fig. 1 Locations of a the main Hawaiian Island chain, b the island of Oahu, and c four study islets (stars) offshore of windward Oahu with varying seabird abundance. Basemap Source: Global Island Database 2015

Stable isotope analysis isotope ratio mass spectrometer (ThermoFinnigan Delta Plus XP IRMS) at the University of California Santa Cruz To assess whether seabird-derived nitrogen could be traced Stable Isotope Laboratory. in adjacent macroalgae, we used nitrogen stable isotope analysis, which has been widely used to map the signal of Data analysis seabird guano in primary producers in terrestrial ecosystems (Anderson and Polis 1999; Schmidt et al. 2004; Croll We categorized islands according to their seabird den- et al. 2005; Young et al. 2010; Szpak et al. 2012). We oppor- sity, with Moku Nui considered “high” and the other three tunistically collected macroalgal samples (n 58) from islets (Mokoli’i, Kapapa, and Popoi’a) considered “low” = the genus Halimeda within the same 45–90 m range our (Table 1). While seabird population numbers fluctuate from water samples were collected in. To establish the isotopic year to year (Amarisa Marie pers comm), average abun- value in algae influenced by anthropogenic nitrogen, we dances in the Mokuluas are an order of magnitude greater collected 8 samples of Halimeda sp adjacent to the main- than the average abundance of Mokoli’i, Kapapa, and land of Oahu (3 m from the Kamehameha Highway) ~9 km Popoi’a. To assess significant differences (α 0.05) in sea- = north of Kaneohe Bay (measured from the middle of the water nutrients between seabird categories (high/low den- Bay at Kapapa Island). We rinsed all thalli with deionized sity), we performed three-way linear mixed effects mod- water to eliminate salt and removed epiphytes and epifauna els using a classic nesting structure where site was nested with forceps. We oven-dried algae at 60 °C for 24–48 h. within islet as a random effect, islet was nested within We ground algae into fine, homogenous powder via mor- seabird category as a random effect, and seabird category tar and pestle and analyzed the algal nitrogen isotopic ratio was a fixed effect. This allowed us to assess the impact (δ15N, ((R /R ) 1) 1000), where R 15N/14N) of seabirds independent of islet. For the same reason, we sample standard − × = using a Carlo-Erba 1108 elemental analyzer coupled to an assessed significant differences in algal δ15N between

1 3 22 Page 4 of 7 Mar Biol (2016) 163:22 seabird categories by using a two-way linear mixed effects model where islet was nested within seabird category as a random effect, and seabird category was a fixed effect. All statistical analyses were performed in Jmp Pro 12.

Results

Seawater nutrients

Mixed effects model results revealed that there were significant differences in dissolved phosphate between high and low seabird categories (F 32.51, P 0.03), and 1,2.003 = = phosphate was greater adjacent to the high seabird islet, Moku Nui, compared to the three low seabird islets (Fig. 2). Fig. 2 Mean dissolved phosphate 1 SE μM, in seawater across In contrast, NOx was not significantly different between islets with low (Mokoli’i, Kapapa,± and Popoi’a) and high (Moku low seabird density islets (mean SE; 0.23 0.09 μM) Nui) seabird density. Different letters imply significant differences ± ± and the high seabird density islet (0.32 0.16 μM; (F1,2.003 32.51, P 0.03) ± = = F 0.26, P 0.66). 1,2 = = Stable isotope analysis

Macroalgae adjacent to Moku Nui (i.e., the high seabird density islet) were significantly enriched in δ15N compared to all other islets (F 23.66, P 0.04; Fig. 3). 1,2.046 = = Mean nitrogen isotopic values ( SD) from samples col- ± lected adjacent to the mainland of Oahu near Kamehameha Highway were much higher than offshore islet samples (8.65 0.94 ‰). ±

Discussion/conclusion

Water samples and macroalgal tissue at coral reefs adjacent to Moku Nui had high values of dissolved phosphate and macroalgal δ15N compared to reefs next to smaller seabird Fig. 3 Mean δ15N SE ‰ of macroalgae from the genus Halim- ± colonies at Mokoli’i, Kapapa, and Popoi’a (Figs. 2, 3). eda across islets with low (Mokoli’i, Kapapa, and Popoi’a) and high Moku Nui has over 5000 nesting wedge-tailed shearwa- (Moku Nui) seabird density. Different letters imply significant differences (F 23.66, P 0.04) ters (Amarisa Marie pers comm), which is over sevenfold 1,2.046 = = the average abundance of the islets in our “low density” seabird category. This suggests that seabird guano may be equaling 7.3 % nitrogen and 1.5 % phosphorus (Smith and delivered in usable forms to nearshore waters and taken up Johnson 1995), and we would therefore predict that seabird by primary producers at Moku Nui. These coral reef results enrichment would be reflected by both elements. In the complement previous work on terrestrial islands (Linde- Aleutian Islands, seabird guano was similarly associated boom 1984; Polis and Hurd 1996; Schmidt et al. 2004; with island-level increases in total soil phosphorus but not Croll et al. 2005; Young et al. 2010), temperate marine sys- soil nitrogen (Croll et al. 2005). Phosphorus can be the lim- tems (Bosman and Hockey 1986; Wootton 1991), and oli- iting nutrient in many carbonate reef environments (Smith gotrophic lagoons (McCauley et al. 2012), indicating that 1984; Lapointe and Clarke 1992). Nutrient limitation on seabirds may provide bottom-up nutrient inputs to a variety coral reefs is predicted to vary depending on geomorphol- of recipient ecosystems. ogy of adjacent islands (Littler et al. 1991) and anthropo- Dissolved nitrate and nitrite values were not differ- genic sources (Cardini et al. 2014), and it may be that the ent between seabird categories. Seabird guano is rich in coral reefs adjacent to Moku Nui are limited locally by both nitrogen and phosphorus, with composition estimates phosphorus but not nitrogen. Northeast trade winds and

1 3 Mar Biol (2016) 163:22 Page 5 of 7 22 high mixing during the sampling season further compli- from samples collected adjacent to our high seabird islet, cate the ability to track differences in seawater nutrients Moku Nui, which is not in Kaneohe Bay. among islets. Regardless, we still found a strong signal for It remains unclear how natural nutrient subsidies from phosphorus in the seawater adjacent to Moku Nui, indicat- seabirds interact with coexisting anthropogenic stressors ing that seabird-derived phosphorus may be retained even that are known to increase nutrient delivery, decrease the during mixing periods. However, the nutrient sampling number of herbivorous fishes, and reduce the overall resil- in this study provides only a snapshot of reef nutrients ience of coral reefs (e.g., Hughes et al. 2003). On Jamaican across space, which may be much different over a longer reefs, nutrient enrichment, disease, and overfishing trans- time scale and during different seasons and environmental formed healthy coral reefs from coral-dominated to algal- conditions. dominated ecosystems (Hughes 1994), while many of the In contrast to the short-term snapshot provided by sea- reefs in the Main Hawaiian Islands are suffering from simi- water nutrient sampling, stable isotope analysis provides a lar threats (Friedlander and DeMartini 2002; Aeby et al. longer-term record of nutrient enrichment in marine pro- 2011). Most Oahu reefs have been and are actively fished ducers (e.g., Costanzo et al. 2005; Mcclelland et al. 1997). (Stimson et al. 2001; Williams et al. 2006, 2011), and natu- Our results indicate that Halimeda δ15N, like phosphate, is ral nutrient subsidies by seabirds may pose an additional enriched at our high seabird islet, Moku Nui, and depleted risk to reefs if primary producers are not sufficiently regu- in δ15N next to islets making up our low seabird category lated by herbivore populations. (Fig. 2). These results support the hypothesis that seabird Nearly a third of all seabird species are at risk of guano provides nitrogen that is taken up by reef primary extinction globally (Spatz et al. 2014), and breeding sea- producers. It is possible that these nutrients are then trans- birds in Oahu are in peril of extirpation. The small islets ferred up the food chain when macroalgae are consumed by in our study are some of the only isolated habitats avail- herbivorous fishes and invertebrates, a result that has been able for burrow-nesting birds like wedge-tailed shearwa- seen on terrestrial islands (e.g., Polis and Hurd 1995). ters, which are extremely vulnerable to human trampling Anthropogenic inputs from mainland Oahu may con- and invasive species (e.g., Young et al. 2013). Seabird found the levels of nutrients found in offshore seawater and conservation efforts in Hawaii have included removing macroalgae. However, the majority of significant anthro- invasive mammals and ants from these islands, and many pogenic nutrient sources in our study area originate in or of these actions have been successful (Smith et al. 2006). near Kaneohe Bay, relatively far from Moku Nui (Fig. 1). However, seabirds are perpetually threatened by species Kaneohe Bay has a long history of nutrient enrichment invasions and disturbance. It is unclear how future sea- from sewage effluent (Smith et al. 1981; Hunter and Evans bird restoration will affect the already heavily impacted 1995). Between 1940 and 1970, sewage from three sepa- reefs in Kaneohe Bay, but our results suggest that it may rate treatment plants was discharged into the bay, fueling increase the delivery of phosphate and isotopically heavy the proliferation of the chlorophyte Dictyosphaeria cav- nitrogen to the surrounding marine environment. It is ernosa while reducing scleractinian coral cover at patch prudent for coral reef managers to consider the potential reefs and fringing reefs prior to sewage diversion in 1980 impacts of increasing or decreasing seabird populations (Smith et al. 1981; Hunter and Evans 1995; Stimson et al. on the islands adjacent to coral reefs. Seabirds naturally 2001). Furthermore, Kaneohe Bay is subject to signifi- occur next to hundreds of coral islands and atolls through- cant intrusion of freshwater runoff from nearby streams, out the globe, but anthropogenic influence may compli- which has resulted in reef kills during extreme storms (e.g., cate the impact of seabird/reef nutrient fluxes on coral Jokiel et al. 1993). Additional point sources of anthropo- reefs that are already overfished and polluted. Our results genic nutrients in Kaneohe Bay include a public restroom show chemical enrichment next to one seabird islet off- at Kualoa Regional Park and Moli’i fish pond, both within shore of Oahu, but continued research on higher trophic 1.5 km of Mokoli’i. These point sources are typically levels at Moku Nui and other reefs adjacent to dense reflected by high macroalgalδ 15N values, and indeed mac- seabird populations in Oahu (e.g., at Moku Manu) will roalgal samples collected near Oahu onsite sewage dis- greatly improve our understanding of guano-mediated posal systems (OSDS) and wastewater injection wells have impacts and elucidate whether there are thresholds in been observed to reach >9 ‰ (Amato 2015). The values seabird abundance and distance from shore that influence of δ15N from macroalgae that we collected adjacent to the coral reef parameters. Further empirical evaluation of the Kamehameha Highway were also in this range. We would ecological influence seabirds have on degraded reefs is therefore expect to see enriched δ15N in macroalgae at our necessary to maximize conservation efficacy and mini- Kaneohe Bay islets if anthropogenic point sources were mize the potential unintended consequences of independ- reaching these areas. However, we only saw enrichment ent marine and terrestrial management.

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Acknowledgments We are grateful to the faculty and staff at the Friedlander AM, DeMartini EE (2002) Contrasts in density, size, and Hawaii Institute of Marine Biology for assisting in the logistics of biomass of reef fishes between the northwestern and the main this work, particularly F. Thomas, R. Toonen, and J. Jones. We thank Hawaiian Islands: the effects of fishing down apex predators. G. Marino for fieldwork assistance. We acknowledge B. Patel, K. Mar Ecol Prog Ser 230:253–264. doi:10.3354/meps230253 Mattingly, R. Tallman, J. Bachellier, D. Pruitt, K. McElroy, K. Kop- Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al (2007) Coral reefs ecky, B. Buttler, and J. Walden for laboratory assistance. We thank R. under rapid climate change and ocean acidification. Science Brainard for suggesting the study site, assistance with experimental 318:1737–1742. doi:10.1126/science.1152509 design, and editing the manuscript. We thank P. Raimondi, D. 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