Hawaiian Hotspots: Enhanced Megafaunal Abundance and Diversity in Submarine Canyons on the Oceanic Islands of Hawaii Eric W

Marine Ecology. ISSN 0173-9565

SPECIAL TOPIC Hawaiian hotspots: enhanced megafaunal abundance and diversity in submarine canyons on the oceanic islands of Hawaii Eric W. Vetter1, Craig R. Smith2 & Fabio C. De Leo2

1 Marine Sciences, Hawaii Paciﬁc University, Kaneohe, HI, USA 2 Department of Oceanography, University of Hawaii at Manoa, Honolulu, HI, USA

Keywords Abstract Biodiversity; habitat heterogeneity; megafauna; source-sink; submarine canyon. Submarine canyons are important sources of habitat heterogeneity on the slopes of continents and islands, but the study of canyon ecology has been lar- Correspondence gely restricted to continental margins. Here we use visual and video surveys Eric W. Vetter, Marine Sciences, Hawaii Pacific from 36 submersible dives to evaluate the role of canyons as abundance and University, 45-045 Kamehameha Highway, diversity hotspots for megafauna in the Hawaiian Archipelago, an island chain Kaneohe, HI 96734, USA. embedded in an oligotrophic ocean. We surveyed megafauna in canyon and E-mail: [email protected] slope settings at depths of 350–1500 m along the margins of four islands: the Accepted: 24 October 2009 low ‘islands’ of Nihoa and Maro Reef, and the high islands of Oahu and Moloka’i. Megafaunal communities in canyons differed significantly from those doi:10.1111/j.1439-0485.2009.00351.x in nearby slope habitats at all depths. Highly mobile fishes and invertebrates were consistently more abundant in canyons than on nearby slopes at the same depth off all islands, suggesting that canyons may be important sources of larvae for surrounding habitats. In the few cases where megafaunal abundances were similar or higher on the slope, the differences were typically driven by higher slope abundance of sessile suspension feeders or animals with limited mobility, i.e. by organisms which are likely to have difficulty with high currents and sediment transport in canyons. Megafaunal species richness and diversity generally trended higher within canyons, especially for the highly mobile taxa. Canyons contained 41 megafaunal species never observed on the slope, and increased estimated regional species richness by 25–30 species, indicating that canyons enhanced beta and gamma (regional) biodiversity. An expected trend of greater enhancement of diversity and abundance in canyons on the margins of high versus low oceanic islands was not observed, although megafauna were generally more abundant in both canyon and slope habitats on the high islands (Oahu and Moloka’i). We conclude that submarine canyons on both low and high islands in the Hawaiian Archipelago may provide keystone structures, enhancing megafaunal abundance, providing source populations for the open slope, and enhancing local and regional species diversity.

providing refugia from predation (Gilinsky 1984; Vetter Introduction 1998), enhanced or alternative food resources (Garrison The role of habitat heterogeneity in supporting biodiver- 1991), spawning areas (Drazen et al. 2003), stress sity is well established both theoretically (Tilman 1999) gradients (e.g. Levin 2003) and substratum diversity (van and empirically (Gilinsky 1984; Freemark & Merriam Rensburg et al. 2002). Increased habitat heterogeneity 1986). Habitat heterogeneity may enhance biodiversity by resulting from anthropogenic habitat fragmentation may

Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH 183 Megafaunal diversity and abundance in oceanic submarine canyons Vetter, Smith & De Leo decrease biodiversity on the landscape scale by reducing as commercially exploited species (e.g. shrimps, lobsters, connectivity, population sizes and resource availability crabs, hagfish, rattail fishes, any species captured with bai- (Saunders et al. 1991), and by increasing vulnerability to ted trap or longline) (Company et al. 2008), as food for predators and ⁄ or parasites (Robinson et al. 1995). Habitat higher trophic levels including marine mammals (Martini fragmentation and resultant diversity declines are com- 1998), as recyclers of fisheries discards, and as pest con- mon in terrestrial ecosystems but appear thus far to be sumers of trapped and hooked fish (e.g. Isaacs & relatively rare in marine ecosystems (e.g. Polunin 2008); Schwartzlose 1975; Hessler et al. 1978; Smith 1985; King thus, habitat heterogeneity in the oceans is expected to 1987; Tagami & Ralston 1988; Britton & Morton 1994; enhance biodiversity on landscape scales. Martini 1998). By concentrating scavengers, canyons may The concept of ‘keystone structures’ has recently been be hotspots of scavenger-based ecosystem services and introduced for terrestrial ecosystems to describe habitat enhanced fisheries yields. features that provide essential shelter and resources for Enhanced food availability may also allow canyons to particular species or assemblages, in the process contrib- play important roles in the feeding and reproduction of a uting fundamentally to habitat heterogeneity (Tews et al. broad range of benthic and demersal species. Because 2004). For example, in the open ocean, seamounts may food-rich patches are critical for recruitment success in provide keystone structures by rising into productive sur- many fish and at least some invertebrate stocks, submar- face waters, yielding ‘benthic islands’ of enhanced food ine canyons may provide important habitats for various availability (Haury et al. 2000) and habitat diversity (e.g. life stages of benthic and demersal fishes and invertebrates hard and soft substrates, zones of flow enhancement, deep along continental margins (Vetter & Dayton 1998, 1999; coral beds; Levin et al. 1994; Fock et al. 2002) in an Company et al. 2008; Vetter, in preparation). Enhanced otherwise pelagic ‘landscape’. Along the slopes of conti- food availability in canyons may be especially important nental margins and islands, submarine canyons are recur- for allowing demersal fish and benthic invertebrates to rent sources of habitat heterogeneity that may also serve reproduce in otherwise relatively oligotrophic regions, as ‘keystone structures’. such as the margins of oceanic islands, including Hawaii Submarine canyons are potential sinks for particulate (Yool et al. 2007). Canyons thus may harbor source pop- materials, including macrophytic debris, organic-rich sed- ulations in a ‘source-sink system’ in which dense, but iments, and particle-bound pollutants moving along localized, concentrations of breeding individuals broadcast shores and across shallow platforms. As a consequence, larvae out to the surrounding slope, enhancing local and canyons often are sites of intense organic enrichment and regional species diversity (Snelgrove & Smith 2002; Rex benthic productivity at shelf and slope depths (Dill 1964; et al. 2005). Canyons could also facilitate speciation by Shepard & Dill 1966; Griggs et al. 1969; Rowe et al. 1982; providing distinct, relatively isolated habitats along more Josselyn et al. 1983; McHugh et al. 1992; Lawson et al. continuous slopes (Levin et al. 2001). 1993; Vetter 1996; Vetter & Dayton 1998). Consumers The role of canyons as biomass and diversity hotspots feeding in canyons, including commercially exploited spe- may be enhanced on the margins of oceanic islands cies, can experience increased food supply through at least embedded in low-productivity open-ocean ecosystems, three mechanisms: suspension feeders benefit from accel- such as in the Hawaiian Archipelago. Even though oce- erated currents (Rowe 1971; Shepard et al. 1974), demer- anic islands and associated canyons are common, the sal planktivores may exploit dense layers of zooplankton importance of canyons as hotspots of enhanced abun- that become concentrated (actively or passively) in can- dance and biodiversity on island slopes remains virtually yons during vertical migrations (e.g. Greene et al. 1988), unstudied. Here we investigate the ecological role of sub- and detritivores benefit from enhanced sedimentation marine canyons on oceanic islands by comparing canyon rates and accumulation of macrophytic and microalgal and slope megafaunal communities within the Main and detritus in canyons (e.g. Rowe et al. 1982; Okey 1993; Northwest Hawaiian Islands. Specifically, we test the fol- Vetter 1994, 1995; Harrold et al. 1998). lowing hypotheses: Canyons may also focus the deposition of nekton car- 1 Megafaunal abundance and local (alpha) diversity are casses, concentrating scavengers (Vetter 1994, 1995). Scav- enhanced in Hawaiian canyons compared to nearby enger populations can contribute significantly to biomass slope habitats. on ocean margins (e.g. Isaacs & Swartzlose 1975; Smith 2 Such canyon enhancement is especially pronounced 1985; Martini 1998; Smith & Demopoulos 2003) and play for the mobile megafauna due to their greater capac- important roles in ecosystem function, e.g. as consumers ity to deal with the strong currents and sediment and dispersers of nutrients from carrion (Dayton & transport within canyons. Hessler 1972; Stockton & DeLaca 1982; Smith 1985; Brit- 3 Canyon enhancement is greater on the margins of ton & Morton 1994; Martini 1998; Smith & Baco 2003), high versus low oceanic islands (because of greater

184 Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH Vetter, Smith & De Leo Megafaunal diversity and abundance in oceanic submarine canyons

export of terrestrial and nearshore production from forms (or atolls) at depths of 200 m and descend to high islands). depths of 2000 m. Nihoa Island is the largest of the 4 Oceanic canyons harbor faunal assemblages distinct NWHIs, with an area of 70 hectares (3 orders of magni- from the open slope, enhancing regional (or gamma) tude smaller than Oahu and Moloka’i). It rises to 273 m biodiversity. with steep terrain and is dry and sparsely vegetated relative to the Main Hawaiian Islands. Nihoa is surrounded by 575 km2 of coral-reef habitat on the remnant of an Material and Methods inactive volcanic cone (http://coris.noaa.gov/about/eco_ essays/nwhi/nihoa.html). Maro Reef is an extensive coral Study sites reef ecosystem covering approximately 1,856 km2 with We used the Hawaii Undersea Research Laboratory a small subaereal portion during low tide (http://ccma (HURL) Pisces IV and V submersibles to make 36 dives server.nos.noaa.gov/ecosystems/coralreef/nwhi/maro.html). in submarine canyons and nearby slope regions within Study of these canyon systems allowed us to explore the the Hawaiian Archipelago. Here we report megafaunal importance of island type (i.e. large high islands versus low diversity and abundance data from video and visual tran- ‘islands’) to the offshore submarine-canyon environment. sects on the islands of Oahu and Moloka’i in the main Hawaiian Islands, and on Nihoa Island and Maro Reef in Data collection and analyses the Northwest Hawaiian Islands (NWHI). The environmental settings for the canyons studied range from high Around Nihoa Island, the distribution of megafaunal fish islands with relatively large terrestrial and marine sources and invertebrates was evaluated using videographic sur- of organic matter (Oahu and Moloka’i) through a low veys employing the methods of Vetter & Dayton (1998). dry island with limited capacity for terrestrial detrital For video surveys, the submersible maintained an altitude input (Nihoa) to an extensive submerged atoll (Maro of 1 m above the seafloor. Megafauna were then Reef), considered functionally to be similar to a small, counted in non-overlapping frame grabs of the lower low ‘island.’ two-thirds of the video frame, with each frame grab cov- The canyon system studied on Oahu (maximum island ering 5m2 of seafloor. Low megafaunal densities forced elevation of 1600 m) is located offshore of Kaneohe Bay a change in protocol to the use of direct visual censusing on Oahu’s eastern shore (Fig. 1). Kaneohe Bay’s watershed of larger areas for the remaining three islands. The differ- is bordered by cliffs rising to 500–850 m and covers ent sampling method used at Nihoa prevented us from approximately 47 km2 (Smith et al. 1981) with annual including the data from Nihoa Island in some analyses rainfall of 100–150 cm (Chave 1973). The Kaneohe Can- because very different spatial scales and numbers of indi- yon rises from a depth of 1900 m and bifurcates at about viduals were sampled. Visual transects were conducted on 1050 m, terminating to the North near Kaneohe Bay’s Maro Reef, Oahu and Moloka’i using a standardized pro- Ship Channel and to the south off the Sampan Channel. tocol in which the pilot maintained a pre-determined An extremely high northeast swell (7 m) during our heading at constant speed of 2 knots and elevation of Oahu cruise forced a relocation of the control (non-can- 2 m above the bottom. The same light combinations were yon) slope site from an area adjacent to the canyon to the used for each transect and observers at the port and star- leeward Oahu coast. Off Moloka’i, two canyon and slope board windows counted into a voice recorder all animals sites were studied off the eastern end of the island’s north visible in two non-overlapping fields on the port and shore between Kalaupapa Peninsula and Papalaua Valley starboard of the submersible; together, the two fields of (Fig. 1). This coast is dominated by 600–800 m sea cliffs view spanned a swath of about 15 m wide. When obsta- with valleys carved by annual precipitation that ranges cles to navigation were encountered (such as canyon from 200 to 400 cm (Culliney 2006). The terrestrial walls) transects were suspended until the standard survey environment here resembles that of East Oahu in being a protocols could be re-established. Only transects with a wet and lushly vegetated coast; however, in contrast to duration of 3 min or longer were included in the analy- Kaneohe, there is no shallow embayment supporting high ses. Measured visibility varied little between the canyon macroalgal production. Additionally, detritus originating and slope transects at each island-habitat combination from terrestrial and nearshore production is shared among with the exception of low visibility within the canyon at the many canyons along this coast (Fig. 1). 350 m off Oahu. Transects were conducted between 10 m Within the NWHI, we collected data from canyons and above and below the target depths for 3–12 min with adjacent slopes on the south sides of Nihoa Island and longer transects divided into replicate 3-min segments. Maro Reef (submerged at high tide) (Fig. 1). Both canyon Thus, a 3-min visual survey covering 2700 m2 was our systems originate on the edges of large carbonate plat- basic unit of sampling. The canyon habitats generally had

Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH 185 Megafaunal diversity and abundance in oceanic submarine canyons Vetter, Smith & De Leo

Maro reef Isobaths (m) 350 2000 650 3000 1000 4000 Moloka’i Nihoa

Oahu

B Canyon C Slope o 23 10’

o Submerged atoll 25 32’ Nihoa 70 0

o 23 06’ o 25 21’

Maro Reef 1050

0 12 Km 0 6 Km o o o o 170 39’ 170 25’ 161 56’ 161 52’

D E

o 21 19’

o 21 31’ Oahu Kaneohe Bay

o 21 12’

Moloka’i Kalaupapai o 21 19’

08 Km 010 Km o o o o 157 56’ 157 44’ 156 60’ 156 53’

Fig. 1. Bathymetric maps of our study sites in the Hawaiian Archipelago. (A) The entire Hawaiian Archipelago with depth contours of 350 m, 650 m and 1000 m indicated (also 1500 m for Oahu). (B–E) The four ‘islands’ with canyon and slope study sites indicated. (B) Maro reef and (C) Nihoa Island in the Northwest Hawaiian Islands. (D) Oahu Island and (E) Moloka’i Island in the Main Hawaiian Islands. Red dots indicate sites at which replicate canyon surveys were conducted; white dots indicate slope sites. Depths are in meters. Multi-beam bathymetric data provided by C. Kelley and J. Smith, from Hawaiian Undersea Research Laboratory (HURL). a limited width of ﬂat bottom appropriate for transecting, were studied at depths of 350, 650 and 1000 m. We also so for most canyon-slope comparisons at a speciﬁc depth, studied 1500-m depths off Oahu and 1200-m depths more transects were completed on the slope. All sites off Nihoa. Still photography, video, and manipulator

186 Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH Vetter, Smith & De Leo Megafaunal diversity and abundance in oceanic submarine canyons collections, as well as the HURL image archive, were used trends. Statistical hypothesis testing was thus limited to to confirm identifications of animals from visual and comparisons of species richness, Shannon diversity, and photographic surveys (cf. Smith 1985). abundance between canyon and slope habitats within a Because of greater sampling effort on the slope, species given island and depth. To maintain an experiment-wise richness analyses were conducted by normalizing total spe- alpha level of 0.05, Holm’s modification of the sequential cies observed or numbers of unique species observed by Bonferroni corrections was used (with the Dunn–Sidak transect duration (Oahu, Moloka’i, Maro Reef), number correction) (Holm 1979). When data violated the para- of video frames (Nihoa), or number of individuals (i.e. metric assumptions of normality and ⁄ or homoscedastic- rarefaction). Percent effort (Table 2) is reported as the ity, natural log transformations were used. When such number of transect minutes (or video frames) in the can- transformation failed to produce normal, homoscedastic yon divided by the number of minutes from the corre- distributions, the non-parametric Mann–Whitney test was sponding slope, so that values less than 100% indicated used. The Mann–Whitney test assumes similar distribu- greater effort on the slope. Relative richness (in Table 2) is tions but is robust to outliers which were resistant to cor- the ratio of normalized richness from the canyon divided rection by transformation in some of our data. PRIMER by that of the slope, resulting in values >100% when can- version 6 was used for diversity analyses with Shannon H’ yon normalized richness exceeded that of the slope. The to base e and rarefaction. Species accumulation curves same technique was used for reporting relative uniqueness. were based on presence–absence data. Mean species accu- Rarefaction curves were plotted using Hurlbert’s (1971) mulation curves (i.e. the average of an infinite number of modification of Sanders (1968) rarefaction for diversity random permutations of ordering) for successive pooling comparisons at the landscape scale (e.g. comparing canyon of habitat types (canyon or slope) across islands were cal- versus slopes by island) to (i) control for the effects of dif- culated using the method of Ugland et al. (2003), and fering sampling effort and faunal densities, and (ii) allow total species richness was estimated using the Chao 1 and the Nihoa data, which sampled much smaller areas using Bootstrap indices as outlined in Magurran (2004) using video transects, to be compared with data from the other PRIMER 6 software. locations where visual transecting was used. SPSS version 13 (Macintosh) was used for ANOVA Results and Mann–Whitney tests. Complex interactions involving both depth and habitat (canyon versus slope) precluded As expected, multifactor analysis revealed strong inter- use of multifactor ANOVA for the examination of general actions between all combinations of the three factors

Fig. 2. Mean abundance per 3-min visual transect by depth and habitat for total megafauna (left figures) and highly mobile megafauna (right figures). Canyon data are shown by dark columns (C), slope data by light columns (S). Highly mobile megafauna consists of teleosts, chondrychthyes, decapods, and cephalopods. Means ± 1 SE are plotted. ****P < 0.0001, ***P < 0.001, **P < 0.01, *P < 0.05, ns, non-significant.

Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH 187 Megafaunal diversity and abundance in oceanic submarine canyons Vetter, Smith & De Leo

Fig. 3. Mean number of total megafaunal species (left figures) and highly mobile megafaunal species (right figures) per 3-min visual transect. Canyon data are shown by dark columns (C), slope data by light columns (S). Error bars represent 1 SE. ****P < 0.0001, ***P < 0.001, **P < 0.01, *P < 0.05, ns, non-significant.

Fig. 4. Mean Shannon Diversity (H¢ to log base e), mean diversity of total megafaunal (left figures) and highly mobile megafauna (right figures) per 3-min visual transect. Canyon data are shown by dark columns (C), slope data by light columns (S). Error bars represent 1 SE. ****P < 0.0001, ***P < 0.001, **P < 0.01, *P < 0.05, ns, non-significant. examined: island, depth, and habitat (canyon versus experiment-wise error rates at 0.05) resulted in clear pat- slope). This precluded use of factorial ANOVA to exam- terns of megafaunal abundance and diversity in canyons ine general trends in megafaunal abundance and diversity. compared to slope habitats at most island-depth combi- Nevertheless, simple pairwise comparisons (maintaining nations (Figs 2–5).

188 Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH Vetter, Smith & De Leo Megafaunal diversity and abundance in oceanic submarine canyons

Fig. 5. Abundance and species richness of megafauna and highly mobile megafauna by habitat (canyon, C and slope, S) and depth at Nihoa Island. All data from each depth ⁄ habitat combination were pooled and normalized to 100 video frames. The normalization process may have inﬂated the estimated species richness for total megafaunal species in the canyon at 650 m, where eight species were observed with only 35 frames of video that met the standardized transect protocol. The values of N indicate the number of frames analyzed at each habitat ⁄ depth combination. Note the change in scale on the y-axis for species richness ﬁgures. No transects were taken on the slope at 1200 m.

Table 1. Patterns in abundance, species richness and Shannon diversity between canyon and slope habitats by different taxonomic or mobility groupings.

No shading indicates higher values observed on the slope, light shading indicates higher values in the canyon, black fill indicates no significant or nearly significant differences. ****P < 0.0001, ***P < 0.001, **P < 0.01, *P < 0.05, filled, non-significant. Numbers indicate probability values that were <0.05 but above the minimum P-value to maintain an experiment-wise error rate of 5%. Tot, total megafauna; Mob, highly mobile megafauna; Fish, all fishes; Crust, all crustacea; Sus, sessile suspension feeders.

to highly mobile taxa off Oahu at 1000 m resulted in a Patterns of abundance change from higher slope abundance (P < 0.01, where the The abundance of total megafauna was not predominantly slope was dominated by sessile sea pens) to no difference, greater in either canyons or on slopes, with three signiﬁ- and at 1500 m a change from greater abundance on the cant differences for particular island–depth combinations slope (P < 0.01, octocorals dominant) to greater abun- favoring canyons, and four favoring slopes (Fig. 2). How- dance in the canyon (P < 0.05). Similar shifts were ever, the highly mobile megafauna (teleosts, chondrychth- observed off Moloka’i and Maro Reef. In general (6 ⁄ 7 yes, decapods, and cephalopods) showed enhancement in cases), mobile megafauna were two to four times more canyons compared to sessile or moderately mobile organ- abundant in canyons than at similar depths on slopes isms. For highly mobile megafauna, seven out of nine com- (Fig. 2). The emergent general pattern from these analyses parisons revealed signiﬁcantly higher canyon abundance is one of greater megafaunal abundance in the canyons with the remaining two comparisons exhibiting non-signif- except where suspension and ⁄ or deposit feeders abounded icant differences (Fig. 2). For example, restricting analyses on the slope (Table 1, Video S1).

Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH 189 Megafaunal diversity and abundance in oceanic submarine canyons Vetter, Smith & De Leo

Fish and crustaceans, which dominated the mobile and 5). We caution that the differences in transecting megafauna category, typically were more abundant in methods prevents direct comparisons (e.g. in absolute canyons. Specifically, in five of the nine island–depth con- abundance) between Nihoa and the other islands, but it trasts, fish were significantly more abundant in canyons, is clear that megafaunal abundance patterns on Nihoa and crustacea were significantly more abundant in can- show greater relative enhancement of the canyon mega- yons in six of nine comparisons (they were never signifi- fauna than on Oahu or Moloka’i. cantly more abundant on slopes; Table 1). Cephalopods were observed more often in canyons off Oahu and Maro Patterns of diversity Reef and were equally abundant in both habitats off Moloka’i. When considered alone, suspension feeders The hypothesis that local (or alpha) diversity would be were significantly more abundant on the slope in four of greater in canyons than on the slope was evaluated using the nine pairwise comparisons and more abundant in comparisons of species richness per normalized area (spe- canyons at three of the island–depth combinations cies counts per transect or frame) and the Shannon Index (Table 1). The data from Nihoa Island collected from (H¢). Higher megafaunal species richness was observed in video could not be compared statistically with the other the canyons in seven of the nine contrasts, with five of three locations (see Material and Methods) and lacked these differences being statistically significant (Fig. 3). sufficient numbers of transects to provide reasonable sta- Species richness on the slope significantly exceeded that tistical power for standard comparisons; however, when in the canyon only at 350 m off Moloka’i (Fig. 3), largely normalized to numbers of animals seen per 100 frames, due to greater numbers of suspension-feeding species there were more than twice as many animals observed in (Table 1). A similar pattern was seen using Shannon canyons as on the slope (Fig. 5). diversity, with the diversity index higher in the canyons The data from both the Main and Northwest Hawaiian in six of nine contrasts (Fig. 4). Two of those differences Islands (Figs 2 and 5) strongly support our Hypothesis 2 were non-significant, but along with the absence of signif- that the abundance of mobile megafauna is especially icantly greater diversity at any of the slope sites, they con- enhanced in canyons relative to slope habitats. However, tribute to an overall pattern of greater diversity in total megafaunal abundance was not generally enhanced canyons. When only highly mobile megafauna were con- in canyons, disproving the abundance component of sidered, there were no island-depth combinations for Hypothesis 1. When higher overall megafaunal abundance which species richness or Shannon diversity were signifi- occurred on slopes, this difference was driven by greater cantly higher on the slope (Figs 3 and 4). The only con- numbers of sessile suspension feeders or echinoderms on trast in which the slope species richness non-significantly the slope (Table 1). The prediction of greater megafaunal exceeded that in the canyon was off Oahu at 1000 m enhancement in canyons on high islands versus low (Fig. 3, Table 2). Other changes in outcomes when islands (Hypothesis 3) was not supported, with both restricting analyses to highly mobile taxa included the Maro Reef and Nihoa (low-relief settings) yielding rela- greater richness and Shannon diversity observed in the tively higher megafaunal abundance in canyons (Figs 2 canyons off Maro Reef at 1000 m becoming statistically

Table 2. Species richness and number of species observed only in either the slope or canyon habitat by island and depth.

Oahu Moloka’i Maro Reef Nihoa

Depth 1500 1000 650 350 1000 650 350 1000 650 1000 650 350

Habitat C ⁄ SC⁄ SC⁄ SC⁄ SC⁄ SC⁄ SC⁄ SC⁄ SC⁄ SC⁄ SC⁄ SC⁄ S

Effort 89% 25% 104% 73% 89% 169% 75% 256% 21% 90% 32% 31% Total species 23 ⁄ 27 24 ⁄ 33 45 ⁄ 42 30 ⁄ 15 67 ⁄ 51 78 ⁄ 35 54 ⁄ 44 40 ⁄ 15 29 ⁄ 44 32 ⁄ 25 8 ⁄ 13 14 ⁄ 8 Relative richness 96% 287% 103% 278% 146% 133% 161% 104% 310% 186% 192% 650% Unique species 18 ⁄ 14 11 ⁄ 20 21 ⁄ 18 21 ⁄ 625⁄ 947⁄ 426⁄ 16 27 ⁄ 215⁄ 30 14 ⁄ 74⁄ 910⁄ 4 Relative uniqueness 146% 216% 112% 489% 300% 725% 218% 557% 231% 300% 138% 1000%

Depth, depth in meters; Habitat, Canyon ⁄ Slope. Effort indicates the number of minutes of transecting or, for Nihoa, the number of video frames analyzed for canyon habitats relative to the corresponding slope. Effort <100% indicates greater sampling effort on the slope. Total species repre- sents the species count for each island–depth–habitat combination with the left value from the canyon(s) and the right from the slope(s). Relative richness is the number of species observed in the canyon relative to the slope after normalization for effort (number of minutes or frames). Unique species are those observed only in the canyon or on the slope for each island–depth combination. Relative uniqueness is the ratio of unique canyon taxa relative to unique slope taxa after normalization for effort.

190 Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH Vetter, Smith & De Leo Megafaunal diversity and abundance in oceanic submarine canyons

Table 3. Dominant megafaunal taxa (% of abundance) in canyons and slopes at our study sites. See notes below table.

350 m 650 m

Site Taxa Canyon (%) Slope (%) Taxa Canyon (%) Slope (%)

Oahu Heterocarpus (D) 69.4 0 Phormosoma sp. (E) 24.6 3.9 Halipterus willemoesi (Cn) 12.7 0 Shrimp (D) 21.8 3.9 Myctophid (T) 3.4 0 Fly-trap anemone 9.2 13.3 (hormathiid ⁄ actinostholid) (Cn) Heterocarpus laevigatus (D) 2.5 0 Macrourids (T) 7.4 11.1 Scorpaenids (T) 2.2 0 Caelorhynchus sp. (T) 3.8 2 Benthic ctenophores (Ct) 0 34.8 Pennatula sp. (Cn) 0 9.5 Sericolophus hawaiiensis (Sp) 0.2 25.1 Ventrifossa sp. (T) 2.9 8.3 Chlorophthalmus sp. (T) 0.1 18.4 Ophiuroids (O) 0.4 7.7 Chascanopsetta prorigera (T) 0.5 4.3 Laganum fudsiyama (E) 0 4.3 Moloka’i Chlorophthalmus (T) 25.7 35.4 Ophiuroids (O) 16.9 0 Myctophid (T) 19.1 0.1 Cerianthids (Cn) 15 4.3 Chrionema chrysalis (T) 7.1 1.7 Shrimp (D) 10.8 4 Synagrops sp. (T) 5.6 1.5 Fly-trap anemone (Cn) 10.4 1 (hormathiid ⁄ actinostholid) Brachyuran crab (D) 3.6 0.3 Phormosoma sp. (E) 7.8 59.4 Sea Pens (Cn) 0.3 18.2 Paelopatides retifer (H) 0.8 6.2 Fungicyathus sp. (Cn) 0 13.1 Nematocarcinus sp. (D) 0.7 4.9 Sericolophus hawaiiensis (Sp) 0 9.1 Synodus sp. (T) 0 3.7 Maro Reef N.D Heterocarpus sp. (D) 20.9 0 Ventrifossa sp. (T) 10.1 1.1 Anemones (Cn) 10.1 0.4 Gorgonians (Cn) 7.4 15 Macrourids (T) 6.1 2.6 Orphnurgus insignis (H) 4.7 19.2 Paelopatides retifer (H) 0 12.4 Shrimp (D) 2 8.5 Sericolophus 0 5.9 hawaiiensis (Sp) Nihoa Myctophid (T) 61.3 0 Teleosts (T) 84.4 30 Gorgonians (Cn) 9.7 0 Pangurids (D) 7.8 0 Orphnurgus insignis (H) 9.7 0 Squalus sp. (Ch) 1.1 0 Ventrifossa sp. (T) 6.5 3.1 Shrimp NOS (D) 1.1 51.3 Macrourids (T) 3.2 21.9 Plesiobatis daviesi (Ch) 0.6 0 Beryx decadactylus (T) 3.2 18.8 Anemones (Cn) 0.6 7.5 Shrimp (D) 0 15.6 Paromola sp. (D) 0 3.8 Teleosts (T) 0 12.5 Neolithodes sp. (D) 0.6 2.5 Anemones (Cn) 0 6.3

1000 m 1500 m

Site Taxa Canyon (%) Slope (%) Taxa Canyon (%) Slope (%)

Oahu Shrimp (D) 33.5 24.4 Bathypeterois atricolor (T) 23.7 1 Aldrovandia sp. (T) 13.4 5.8 Synaphobranchids (T) 14.2 0.5 Sclerasterias sp. (A) 10.4 0 Shrimp (D) 6.8 5 Cerianthids (Cn) 8.5 0.9 Aristeus sp. (D) 6.8 0 Macrourids (T) 4.3 6.1 Plesiopenaeus sp. (D) 4.7 1.4 Halipterus willemoesi (Cn) 0.6 41.3 Anthomastus sp. (Cn) 0 74.6 Paelopatides retifer (H) 3 4.8 Aldrovandia sp. (T) 3.7 3.6 Pennatula sp. (Cn) 0 2.2 Halipterus willemoesi (Cn) 0 1.9

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Table 3. (Continued).

1000 m 1500 m

Site Taxa Canyon (%) Slope (%) Taxa Canyon (%) Slope (%)

Moloka’i Shrimp (D) 21.2 2.4 N.D Aldrovandia sp. (T) 17 1 Paelopatides retifer (H) 11.7 3.3 Ophiuroids (O) 6 42 Macrourids (T) 5.7 0.5 Astroschema sp. (E) 0.4 28.8 Soft corals (Cn) 0.1 3.6 Fungicyathus sp. (Cn) 0 3.6 Maro Reef Paelopatides retifer (H) 19.5 2.5 N.D Aldrovandia sp. (T) 9.8 9.4 Sea Pens (Cn) 9.1 14.8 Dyctyaulus sp. (P) 8.1 0.5 Sericolophus hawaiiensis (Sp) 7.9 13.3 Macrourids (T) 7.8 16.7 Gorgonians (Cn) 1 11.3 Nihoa Shrimp (D) 30.5 19.2 N.D Sea Pens (Cn) 13 1.4 Anemones (Cn) 8.1 6.8 Heterocarpus sp. (D) 8.1 0 Aldrovandia sp. (T) 6.1 15.1 Gorgonians (Cn) 6.1 16.4 Macrourids (T) 4.9 5.5

Shading highlights the top 5 dominant taxa in each habitat. Letters in parentheses identify highly mobile taxa as: Teleosts (T), Chondrychthyes (Ch), Decapods (D), Cephalopods (Cp), and sedentary or sessile taxa as: Sponges (Sp), Cnidarians (Cn), Ctenophores (Ct), Holothuroids (H), Echinoids (E), Ophiuroids (O), Crinoids (Cr), Asteroids (A), Gastropods (G), Polychaetes (P), Cirripeds (C). significant, although off Moloka’i formerly highly signifi- effort on the slope greatly exceeded that in the canyon. cant differences favoring the canyons at 650 and 1000 m When corrected for effort, the relative species richness in became non-significant (Fig. 3). In conclusion, data from the canyons greatly exceeded that on the slope in nine of the Main Hawaiian Islands and Maro Reef generally 12 comparisons and was essentially equal in the remain- showed higher species richness and Shannon diversity in ing three. When the analysis is limited to species unique canyons for total and mobile megafauna; no general to canyons or to the slope, more unique species were canyon versus slope pattern was evident for suspension observed in the canyon in nine of 12 contrasts without feeders when examined alone (Table 1). correcting for effort. After correcting for effort, relative Off Nihoa island, species richness was greater in the uniqueness was greater in the canyons for each contrast canyon at 350 m and 650 m, but greater on the slope at and much greater (38% or more) in all but one compari- 1000 m. After normalizing for sampling effort, species son (Table 2). richness in the canyon exceeded that of the slope for all While striking, the greater numbers of unique species depths (Table 2). When only mobile megafauna were in canyons could be driven largely by rare taxa. Examina- considered, more species were observed in the Nihoa tion of the dominant taxa for each island–depth compari- canyon at all depths (Fig. 5). son revealed that many of the dominants in one habitat Species richness and the number of unique species at are absent or rare in the other (Table 3). For example, off each island–depth combination are presented in Table 2. Oahu at 350 m, there were no shared species among the Sampling effort in canyons exceeded that on slopes by five dominant taxa observed in both habitats. Similarly, at 10% or more only twice, whereas effort on the slope 350 m off Moloka’i, the second through fifth most domi- exceeded that in canyons in nine canyon–slope contrasts. nant taxa diverged strongly between habitats. In a com- This was a result of the limited extent of the canyon parison of the five most abundant species at 650 m, two habitat for a given island and depth. The total number of taxa were shared off Oahu, three off Moloka’i, and one species observed in the canyons was greater in all three off Maro Reef and Nihoa (Table 3). More dominant taxa instances where canyon effort exceeded that on the slope. were shared between the slope and canyon at 1000 m, but The same was true for five of the nine comparisons when this may have been partially due to lumping several

192 Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH Vetter, Smith & De Leo Megafaunal diversity and abundance in oceanic submarine canyons species together as shrimp, sea pens, or anemones. The habitats. These data demonstrate that the canyon and only comparison at 1500 m (Oahu) revealed that only slope habitats diverge strongly both in the species assem- one of the ﬁve most abundant taxa was shared between blages they support and in the dominant species. Taken together these data strongly support Hypothesis 4, i.e. A that oceanic canyons harbor faunal assemblages distinct 200 All taxa from the open slope, increasing both the variety of habitat types (beta diversity) and regional (gamma) diversity (Ricklefs & Miller 1999). 150 Analyses of species accumulation and richness at the full canyon or slope scale with all depths combined (i.e. at the ‘landscape’ scale) also indicated higher species richness, and distinct faunal assemblages, in canyons com- 100 pared to the open slope. The mean species accumulation curve for all taxa in canyons remained substantially (20 Species richness species) above that for the slope sites (Fig. 6A). Both 50 Canyon + Slope curves very nearly reach an asymptote, suggesting that Canyon both canyon and slope systems were well sampled Slope (Fig. 6A). Estimated total species richness was also greater

0 for canyons by 10–15 species, depending on the index 12345 used (Fig. 6B). Finally, species accumulation curves con- Sites pooled sidering only species unique to canyons or to slopes B 240 revealed considerably more species unique to canyons All taxa than to slopes (Fig. 6C). Forty-one species were only

200 observed in canyons, suggesting that canyon and slope species lists show substantial non overlap, and that canyons are contributing substantially to beta and gamma 160 (regional) diversity. The enhancement of regional diversity resulting from the presence of canyons is indi- 120 cated by comparing species accumulation curves (Fig. 6A)

Bootstrap and species richness estimates (Fig. 6B) for combined Species richness 80 Chao1 canyon plus slope data with those for the slope alone. Canyon + Slope Both approaches suggest that the presence of canyon hab- 40 Canyon itats in the Hawaiian Archipelago increases the regional Slope megafaunal species pool by 25–37 species above the level

0 supported by slope habitats alone. 12345 Rarefaction curves plotted at the landscape scale (i.e. Sites pooled by island and habitat with all depths pooled) provided C 40 additional insights into the inﬂuence of canyons on me- Unique taxa gafaunal species diversity. The initial portions of canyon curves (i.e. at levels below 50 individuals) fell below

Fig. 6. (A) Mean species accumulation curves for all megafaunal taxa and all depths, for canyons, adjacent slopes, and canyon + slope data 20 combined. The curves indicate mean species accumulation (Magurran Canyon Slope 2004) as the number of sites is successively increased. (B) Estimated total megafaunal species richness in canyon habitats, slope habitats, Species richness and canyon + slope habitats combined (all depths at each site 10 pooled), as the number of pooled sites is successively increased, using Chao 1 and Bootstrap estimators. (C) Mean accumulation of taxa unique to canyons or slopes as the number of pooled sites is increased. ‘Unique’ canyon or slope taxa were only observed in can- 0 12345 yon or slope habitats, respectively, in this study. Sites are: Moloka’i Sites pooled East, Moloka’i West, Oahu, Maro and Nihoa.

Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH 193 Megafaunal diversity and abundance in oceanic submarine canyons Vetter, Smith & De Leo

120 100 Maro Reef Moloka’i 100 80 80 60 60 40 40 20 20 0 0 10 210 410 610 810 1010 1210 1410 1610 10 230 450 670 890 1110 1330 1550 1770 1990

100 Oahu 60 Nihoa 80 50 Fig. 7. Hurlbert rarefaction curves for total megafauna observed at each island in canyon 60 40 Expected number of species 30 habitats (solid blue lines) and slope habitats 40 Combined (dotted red lines), and for the canyon + slope 20 Canyon 20 Slope data combined (solid black lines). In all cases 10 the combined canyon + slope curve lies above 0 0 10 230 450 670 890 1110 1330 1550 1770 1990 10 80 150 220 290 360 430 500 570 640 the slope curve, indicating that canyons Number of individuals contribute to gamma diversity. slope curves, reflecting greater species dominance in can- canyon off Maro Reef (F. De Leo, E. Vetter and C. Smith yon habitats at all islands but Moloka’i, where stronger unpublished data). The enhancement of mobile mega- dominance was observed on the slope (Fig. 7). By levels fauna, especially fish, in Hawaiian canyons is similar to of 200–700 individuals, however, canyon curves had the findings of enhanced mobile megafauna in other crossed the slope curves, indicating higher species rich- canyon systems, including numerous canyons on the ness in canyon systems in agreement with the Chao 1 California margin (Vetter & Dayton 1999; E. Vetter and Bootstrap species-richness estimators (Fig. 6B). unpublished data), in the Western Mediterranean When canyon and slope data were pooled for individual (Stefanescu et al.1994), and in Pribilof Canyon, Alaska island margins, the pooled curve invariably fell above the (Brodeur 2001). slope curve for each island, indicating that the presence Elevated abundance of scavenging fish and crustaceans of the canyon habitat enhanced regional megafaunal in canyons in the Main and Northwest Hawaiian Islands diversity (Fig. 7). suggests that those habitats experience greater food avail- In summary, analyses of species biodiversity at a variety ability, as has been observed in many canyons on conti- of scales suggest that local megafaunal diversity is nental margins (Greene et al. 1988; Vetter & Dayton enhanced in canyons compared to nearby slope habitats, 1999; Hooker et al. 2002; Cotte´ & Simard 2005). Because and that the canyons support faunal assemblages distinct food-rich patches are critical for recruitment success in from the open slope, enhancing beta and gamma many fish stocks, submarine canyons may provide impor- (regional) biodiversity. These results again strongly sup- tant habitats for food-limited life stages of benthic and port our Hypothesis 4. demersal fishes (Stefanescu et al. 1994; Vetter & Dayton 1998, 1999; Yoklavich et al. 2000; Brodeur 2001; Vetter in preparation). Along the California and Mediterranean Discussion coasts, submarine canyons are regularly targeted by com- Contrary to our Hypothesis 1, we found no general pat- mercial and recreational fisherman exploiting rockfish, tern in megafaunal abundance between the canyon and rattails, other bottom fishes and invertebrates (C. Smith slope habitats when all taxa were considered; however, and E. Vetter unpublished observations; Company et al. the greater abundance of mobile megafauna in canyons 2008). The enhanced abundance of fish in Hawaiian can- strongly supported our second hypothesis that animals yons documented in this study, together with observa- capable of dealing with physical disturbance would benefit tions of fishing effort targeting Moloka’i canyons (C. most from canyon conditions (e.g. higher food availabil- Kelly personal communication), suggests that canyons ity). Evidence for disturbance in canyons observed in this may provide critical habitat for bottom fishes in the study included large ripple marks in canyon sediments, Hawaiian Archipelago as well (e.g. lutjanid snappers and coarser sediments, large patches of terrestrial detritus synaphobranchid eels). deep in canyons off Moloka’i (Videos S2 and S3), large The majority of fishes and crustaceans observed in numbers of algal aggregates moving down-canyon off deep-sea canyon and slope habitats are considered to be Oahu (observed from 350 to 1500 m (Videos S4 and scavengers that may benefit from funneling of nekton car- S5)), and accumulations of green algae at 350 m in the casses (food-falls) in canyons. For example, in a baited

194 Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH Vetter, Smith & De Leo Megafaunal diversity and abundance in oceanic submarine canyons camera study, King et al. (2008) reported similar numbers are the likely causes of increased numbers of mobile ani- of scavengers in the Nazare´ canyon off Portugal as on the mals in canyons; however, many factors such location, Porcupine Abyssal plain, which is found beneath much distance from shore, orientation to currents, overlying more productive waters. They found that scavengers production regime, etc., can result in differences between arrived later and remained longer near bait at a single and within canyons. One goal of continued research in camera deployment at the abyssal plain (4437 m) than in submarine canyons should be to determine which char- the canyon and cautiously suggested that this could indi- acteristics of canyons, such as focusing of detritus cate a greater food supply in the canyons. De Leo, Smith, originating in shallow water, increased current ﬂows, and Vetter (in preparation) often caught greater numbers and concentration of vertically migrating organisms and biomass of scavengers (mostly Heterocarpus shrimp (Video S6), are particularly important for enhancement and lysianassid amphipods) in traps deployed in canyons of megafaunal abundance. Ultimately, a classiﬁcation at the Hawaiian canyons studied here. There is thus a system integrating geological, biological oceanographic, recurrent trend of greater abundance of mobile mega- and hydrographic conditions in canyons could prove fauna in canyons than on nearby slopes of equivalent useful to predicting patterns of megafaunal enhancement depths. Increased food availability and ⁄ or habitat diversity in submarine canyon.

Table 4. List of shared and unique taxa combining all submarine canyons and slopes studied off Main and Northwest Hawaiian Islands during this study.

Shared species Canyon exclusive species

Fishes Invertebrates Shrimp Fishes Etelis caruscans (T) Gadomus melanopterus (T) Sericolophus hawaiiensis (Sp) Lepadimorph (C) Caelorhynchus aratus (T) Invertebrates Caelorhynchus doryssus (T) Dyctyaulus sp. (P) Neolithodes sp. (D) Malacocephalus sp. (T) Regadrella sp. (P) Coryphaenoides sp. (T) Dactylocalcid vase (P) Acanthophyra sp. (D) Ophidiid (T) Histocidaris sp. (E) Ventrifossa sp. (T) Actinostolid (Cn) Sclerasterias sp. (A) Luciobrotula bartschi (T) Polymastia sp. (Cn) Nezumia sp. (T) Hormathiid (Cn) Astropecten sp. (A) Synaphobranchus afﬁnis (T) Lyrocteis sp. (Ct) Aldrovandia sp. (T) Cerianthid (Cn) Brisinga sp. (A) Pycnocraspedum armatum (T) Walteria sp. (P) Meadia abyssalis (T) Coralomorphus sp. (Cn) Anthenoides sp. (A) Lamprogrammus brunswegii (T) Bathypathes sp. (D) Nettastoma sp. (T) Anthomastus sp. (Cn) Asteroschema sp. (O) Saurenchelys sp. (T) Cirrhipathes sp. (Cn) Ijimaia sp. (T) Cirrhipathes sp. (Cn) Araeosoma sp. (E) Gempylus sp. (T) Iridogorgia bella (Cn) Plesiobatis daviesi (Ch) Nerella sp. (Cn) Aspidodiadema sp. (E) Apristurus spongiceps (T) Halipterus willemoesi (Cn) Squalus sp. (Ch) Iridogorgia superba (Cn) Stereocidaris hawaiiensis (E) Symphysanodon moanaloae (T) Heterocarpus laevigatus (D) Centroscyllium sp. (Ch) Pennatula sp. (Cn) Laganum fudsiyama (E) Chaunax sp. (T) Caenopedina pulchella (E) Hydrolagus purpurescens (Ch) Umbellula sp. (Cn) Paelopatides retifer (H) Lophiodes miacanthus (T) Clypeaster leptostracon (E) Beryx decadactylus (T) Benthesicymus (Cr) Orphnurgus insignis (H) Sphoeroides pachygaster (T) Phormosoma bursarium (E) Bathypeterois sp.1 (T) Brachyuran crab (D) Mesothuria parva (H) Laemonema sp. (T) Enypniastes sp. (H) Bathypeterois sp.2 (T) Galatheid crab (D) Mesothuria carnosa (H) Bembrops sp. (T) Antedon sp. (Cr) Sladenia remiger (T) Paromola sp. (D) Octopus sp. Seriola dumerii (T) Xenophyophore sp. Satyrichthys engycerus (T) Pangurid (D) Squid Rexea nakamurai (T) Goniasterid (A) Tadpole ﬁsh (T) Parapagurus sp. (D) Pleurobranchid (G) Etelis carbunculus (T) Phalium sp. (G) Pontinus macrocephalus (T) Randallia distincta (D) Gastropod sp. Myctophid (T) Chascanopsetta prorigera (T) Heterocarpus (D) Henricia sp. (A) Apogonid (T)

Chrionema chrysalis (T) Aristeus sp. (D) Conus sp. (G) Slope exclusive species

Chlorophthalmus sp. (T) Plesiopenaeus sp. (D) Tunicate FISHES Epigonus sp. (T) Glossanodon struhakeri (T) Nematocarcinus sp. (D) Polynoid (P) Aldrovandia phalacra (T) Barbourisia rufa (T) Parapercis roseoviridis (T) Plesionika sp. (D) Aldrovandia verticalis (T) INVERTEBRATES Polymyxia sp. (T) Cyrtomaia smithi (D) Hexatrygon bickelli (T) Liponema sp. (Cn) Synagrops sp. (T) Bathygadid (T) Fungyciathus sp. (Cn) Bathytyphlops marionae (T) Solaster sp. (A) Hoplichthys citrinus (T) Phryssocystis sp. (E) Poecillopsetta hawaiiensis (T) Spatangoid (E) Synodus sp. (T)

Letters in parentheses identify highly mobile taxa as: Teleosts (T), Chondrychthyes (Ch), Decapods (D), Cephalopods (Cp), and sedentary or sessile taxa as: Sponges (Sp), Cnidarians (Cn), Ctenophores (Ct), Holothuroids (H), Echinoids (E), Ophiuroids (O), Crinoids (Cr), Asteroids (A), Gastropods (G), Polychaetes (P), Cirripeds (C).

Marine Ecology 31 (2010) 183–199 ª 2010 Blackwell Verlag GmbH 195 Megafaunal diversity and abundance in oceanic submarine canyons Vetter, Smith & De Leo

Our hypothesis that megafaunal diversity is enhanced ated physical disturbance. The large numbers of mega- in Hawaiian canyons compared to nearby slope habitats faunal fishes and crustaceans we observed in canyons was supported by a strong trend of elevated species should be able to avoid or overcome canyon-associated richness and Shannon diversity in canyons. These greater slumps and currents, allowing them to benefit from values could result from far-ranging organisms remaining organic material transported from shallower depths with longer in canyons because of more food or desirable habi- these events as in Mediterranean canyons (Company tat features; larger population sizes resulting in a greater et al. 2008). likelihood of inclusion in surveys; more canyon special- The hypothesis that oceanic canyons function as hot- ists; and the use of canyons as nurseries or spawning spots of biodiversity by harboring faunal assemblages grounds. Canyon assemblages were observed to be more distinct from the slope was supported by the long list of uniformly speciose, whereas the slopes frequently had species observed only in canyons (Table 4). This large tracts with few species or individuals interrupted by together with (i) the smaller list of species only observed patches of plenty. At some slope sites, it was not unusual on the slope and (ii) the enhancement of species rich- to travel 100 m or more observing little other than sedi- ness and rarefaction diversity when canyon and slope ment and then to encounter rocky outcrops with high habitats were pooled (Figs 6 and 7) demonstrates that abundance and species richness (e.g. an outcrop with fish, submarine canyons on islands in oligotrophic oceans crabs, and shrimp which was encountered after traveling may contribute substantially to both beta and gamma >500 m without seeing any megafauna; Video S7). These diversity. The higher abundance and species richness of rocky habitats appear comparable to other habitat oases fish and crustaceans often found in the Hawaiian can- such as isolated trees in the African savanna (Milton & yons suggest that canyons may also harbor larval-source Dean 1995). Hecker (1994) attributed pronounced patchi- populations and provide a critical habitat for a variety ness of benthos on the slope of Cape Hatteras to a com- of mobile species. Canyons are thus likely to provide bination of habitat heterogeneity, enhanced nutrient keystone structures resulting in hotspots of biodiversity, availability, and a fauna largely composed of sedentary meriting special attention in coastal management and organisms. We found increased abundance and diversity environmental protection from human impacts resulting of highly mobile animals in canyons where hard and soft from bottom trawling, waste disposal, and dredge or substrate were both virtually always visible from the sub- mine spoil dumping on island margins (Smith et al. mersibles, and greater patchiness in animal distributions 2008). on the slope where small islands of hard substrate were often widely separated in a ‘sea’ of sediments. These Acknowledgements results are similar to those of Hargrave et al. (2004) where current speed and substrate composition were We thank R. Martini, J. Drazen, C. Berini, A. Halberg, found to be major determinants of biodiversity and the N. Rothe, B. Kivi, D. Vardeh, T. Kirby, and the Pisces dominant trophic modes observed in the Gully submarine IV and V crew of the Hawaii Undersea Research Lab canyon in the NW Atlantic. for expert operations of the Pisces IV and V submers- We observed aggregations of suspension feeders ibles within the challenging environment of the submar- (mostly cnidarians and ophiuroids) in both canyon and ine canyons and the captain and crew of the R ⁄ V slope habitats; however, large and dense aggregations of Ka’imikai-o-Kanaloa. The suggestions of two anonymous sessile organisms in sedimentary environments were reviewers substantially improved the final manuscript. only seen on the slope (especially sea-pens, Pennatuli- This work was supported by grants from NOAA Ocean dae). Lower abundance and ⁄ or diversity of sedentary Exploration Office Grant # NA03OAR4600109 and by and sessile organisms in some canyons or portions of the Hawaii Undersea Research Laboratory. 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populations in submarine canyons. Marine Ecology Progress Video S4 Loose detritus and the caridean Heterocarpus Series, 186, 137–148. encifer at 350 m in a submarine canyon off Oahu’s East Yoklavich M, Greene H. G, Cailliet G, Sullivan D, Lea R, Love shore. M (2000) Habitat associations of deep-water rockfishes in a Video S5 Detrital aggregations observed in a submarine submarine canyon: an example of a natural refuge. Fishery canyon off Oahu’s East shore. Similar detrital aggregates Bulletin, 98, 625–641. were seen moving down the canyon or wedged in rocks Yool Y, A. P. Martin A. P, Fernandez C, Clark D. R. (2007) from 300 to 1500 m. The significance of nitrification for ocean production. Nat- Video S6 Myctophid school observed at 432 m in a ure, 447, 999–1002. submarine canyon off the North shore of Moloka’i. Similar aggregations were observed deeper in the same Supporting Information canyon and within canyon systems in the Northwest Additional Supporting Information may be found in the Hawaiian Islands. online version of this article: Video S7 An isolated rocky outcrop in a broad Video S1 Suspension feeding Ophiuroids on the slope sediment plain at 350 m on the slope of Nihoa Island. at 670 m off the North shore of Moloka’i. Please note: Wiley-Blackwell Publishing are not respon- Video S2 Woody debris at 572 m in a submarine can- sible for the content or functionality of any supporting yon off the North shore of Moloka’i. materials supplied by the authors. Any queries (other Video S3 Kukui nuts (Aleurites moluccana) observed at than missing material) should be directed to the corre- 478 m in a submarine canyon off the North shore of sponding author for the article. Moloka’i.

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