Progress in Oceanography 123 (2014) 54–63

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Progress in Oceanography

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Bathymetric patterns of a and b diversity of harpacticoid copepodsat the genus level around the Ryukyu Trench, and turnover diversitybetween trenches around Japan

http://dx.doi.org/10.1016/j.pocean.2014.02.0070079-6611/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author. Tel.: +81 4 7136 6174.E-mail address: tkitahashi-10a@nenv.k.u-tokyo.ac.jp (T. Kitahashi).

Tomo Kitahashi a,⇑, Kiichiro Kawamura b, Shigeaki Kojima a, Motohiro Shimanaga c

a Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japanb Graduate School of Science and Engineering, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8511, Japanc Aitsu Marine Station, Center for Marine Environment Studies, Kumamoto University, 6061 Aitsu, Matsushima, Kami-Amakusa, Kumamoto 861-6102, Japan

a r t i c l e i n f o

Article history:Received 21 August 2013Received in revised form 25 February 2014Accepted 25 February 2014Available online 11 March 2014

a b s t r a c t

The diversity of harpacticoid copepods was investigated around the Ryukyu Trench (430–7150 m), whichlies below an oligotrophic subtropical ocean. The a diversity, which is based on the number of genera andShannon diversity decreased with increasing water depth. The community structure of harpacticoidsgradually changed as the water depth increased from the bathyal zone to the hadal zone. Turnover (b)diversity values were equally high between the trench slope, trench floor and abyssal plain. We comparedthe harpacticoid assemblage obtained from the Ryukyu region with the assemblage from a region aroundthe Kuril Trench (Kitahashi et al., 2013). Turnover diversity values between the two regions (d diversity)were relatively low at shallow depths, but they increased with increasing water depth and reached theirmaximum between the trench floors and abyssal plains. These findings indicate that the bathymetric pat-terns of harpacticoid assemblages differ among regions and that these discrepancies reflect differences inenvironmental conditions, such as primary productivity level.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Biodiversity in the deep sea is considered to be as high as that intropical rain forests (Grassle, 1989). There are two major trends indeep-sea biodiversity, latitudinal and bathymetric gradients (Rexet al., 2005; Rex and Etter, 2010; Tittensor et al., 2010). The formerterm refers to the decline in deep-sea diversity towards the poles(e.g. Rex et al., 1993; Lambshead et al., 2002; Yasuhara et al.,2012), and the latter refers to the parabolic pattern of diversitywith increasing water depth (e.g. Rex, 1981; Etter and Grassle,1992; Paterson and Lambshead, 1995), although there have beenexceptions (e.g. Ellingsen and Gray, 2002; Tittensor et al., 2010;Brault et al., 2013; Trebukhova et al., 2013). It has been suggestedthat these patterns are regulated by the organic flux, which isscarce on the deep sea floor (e.g. Levin et al., 2001; Rex and Etter,2010). Most studies, however, have focused only on bathyal andabyssal depths. Studies extending into the hadal zone (>6000 m)are limited, due to the remoteness of this zone and the difficultyof accessing it (Angel, 1982).

The hadal zone, which refers to narrow, elongated depressions onthe sea floor (trenches) associated with a subduction zone (Jackson,

1997), presents one of the last frontiers of deep-sea exploration (Rexand Etter, 2010). The physical parameters, such as temperature,salinity and oxygen, remain constant and are similar to those foundat shallower depths in the deep sea (e.g. Jamieson et al., 2010).However, the biotic parameters such as the quantity and quality offood (organic matter) supplied from the euphotic zone is drasticallydifferent at the spatial scale of several hundred kilometers aroundtrenches (Boetius et al., 1996; Danovaro et al., 2003; Itoh et al.,2011). Therefore, trenches provide ‘natural experiments’ (Angel,1982) where the effect of food availability on animal assemblagesin the deep sea may be examined.

Harpacticoids are usually the second most abundant metazoanmarine meiobenthic taxon, after nematodes (Giere, 2009), and aresuccessful in the deep-sea environment (Thistle, 2001). However,although some studies have reported changes in the spatial distri-bution of deep-sea harpacticoid copepods (e.g. Baguley et al., 2006;Gheerardyn and Veit-Köhler, 2009; Gheerardyn et al., 2010; Men-zel et al., 2011; Menzel and George, 2012), information regardingharpacticoid assemblages around trenches remains scarce. Jumarsand Hessler (1976) reported that harpacticoid diversity in theAleutian Trench was lower than that on the abyssal plain in thecentral North Pacific. Kitahashi et al. (2013) detected a parabolicpattern of harpacticoid diversity and noted that there are gradualchanges in the distribution of harpacticoid genera from the bathyal

T. Kitahashi et al. / Progress in Oceanography 123 (2014) 54–63 55

zone to the hadal zone around the Kuril Trench, in the north-westPacific.

In the present study, we described the bathymetric patterns ofharpacticoid diversity (a diversity) and community structure (bdiversity) at the genus level around the Ryukyu Trench, which liesbelow an oligotrophic subtropical ocean (cf. Berger, 1989; NASASeaWiFS Project). To examine the effect of the primary productivitylevel on the changing patterns in a and b diversity, we also com-pared these patterns with those around the Kuril Trench (d diver-sity, Kitahashi et al., 2013), 2000 km away, which is locatedbelow a highly productive boreal region. It has been suggested thatfood supply (Soltwedel, 2000; Baguley et al., 2006) and grain size(Montagna, 1982) affect the distribution patterns of meiofauna inthe deep sea. Therefore, we also investigated the associations be-tween environmental factors and harpacticoid assemblages.

2. Materials and methods

2.1. Sampling and sample processing

The samples were collected from a region around the RyukyuTrench, hereafter called the Ryukyu region, during two cruises ofthe research vessels Hakuho Maru (KH05-1) and Tansei Maru(KT10-23) in 2005 and 2010, respectively (Table 1). We used amultiple corer (Barnett et al., 1984) which can simultaneously col-lect up to eight sediment cores of 52.8 cm2. Sampling stations werelocated along the transects descending from the continental mar-gin into the Ryukyu Trench and traveling onto the adjacent abyssalplain, although the southern transect did not cover the abyssalplain (Fig. 1, Table 1). To compare harpacticoid assemblages ob-tained from the present study with those from the Kuril Trench(Kitahashi et al., 2013), we classified the sampling stations into fivetopographical settings (Table 1): bathyal (depth < 1000 m), uppertrench slope (1000–3000 m), lower trench slope (3000–6000 m),trench floor (depth > 6000 m) and abyssal plain (flat topographyseawards from the trench). At each of the stations RT1003 andRT1004, two multiple corer deployments were conducted, withfour cores per deployment were analyzed. For other stations, onemultiple corer deployment was conducted at each station, withthree cores per deployment, because of limited ship time and highdemand for cores (Table 1).

On the ship, a small amount of sediment (<1 mL) was takenfrom the top sediment layer of three or four cores per deploymentin order to determine the chloroplastic pigment equivalent (CPE),the ratio of chlorophyll a to phaeopigments (Chl a/phaeo), mediandiameter (MD) and sorting coefficient (SC) of the sediment grain

Table 1Locations and topographical settings of the sampling stations in the Ryukyu region.

Setting Station Date Latitude

Bathyal RT1004A 20 October 2010 26�20.000 NBathyal RT1004C 20 October 2010 26�20.010 NUpper trench slope PS08 24 May 2005 26�20.140 NUpper trench slope RT1002 20 October 2010 25�29.920 NUpper trench slope RT1003B 20 October 2010 25�29.990 NUpper trench slope RT1003A 20 October 2010 25�30.010 NUpper trench slope RT05 19 May 2005 25�00.110 NUpper trench slope PS07 24 May 2005 26�20.050 NLower trench slope PS06 23 May 2005 26�05.980 NLower trench slope RT03 17 May 2005 24�33.360 NLower trench slope PS05 23 May 2005 26�17.670 NLower trench slope RT04 18 May 2005 24�53.040 NLower trench slope PS04 23 May 2005 26�08.790 NAbyssal plain PS01 10 May 2005 26�04.000 NAbyssal plain PS02 21 May 2005 25�59.960 NTrench floor PS03 22 May 2005 26�12.220 NTrench floor RT01 16 May 2005 24�29.740 N

size (see below). After that, the upper 1 cm of each core sample,where most harpacticoids inhabit (Itoh et al., 2011), was removed.Each sample was fixed and preserved in 5% buffered seawater for-malin and stained with Rose Bengal (final concentration, 0.05 g/L)within several hours of collection, until sample processing in thelaboratory.

In the laboratory, samples from stations PS01–08, RT01 andRT03–05 were sieved using mesh nets of 1.0, 0.5, 0.25, 0.125 and0.063 mm. The residues retained on smaller mesh (<1.0 mm) weretransferred to flat-bottomed petri dishes and harpacticoids werepicked up with an Irwin loop from residues. All samples werechecked for harpacticoids several times. Sediment samples col-lected from the other stations (RT1002–1004) were treated as de-scribed by Danovaro (2010). These sediment samples were passedthrough a 1 mm mesh sieve and retained on a 0.063 mm meshsieve. The sediments remaining on the latter mesh sieve wereresuspended with colloidal silica (Ludox HS40, Sigma–Aldrich;density, 1.31 g/mL) and centrifuged for 10 min at 3000 rpm(1680 G) three times. The supernatants were transferred to flat-bottomed petri dishes and harpacticoids were picked up with an Ir-win loop. The residual sediments of one core from each deploy-ment were also checked to test extraction efficiency.

The developmental stages of all specimens were determinedusing a binocular stereoscopic microscope. Adult specimens wereidentified to the genus level using a compound microscopeequipped with differential interference optics by referring to re-cent literature (Huys et al., 1996; Boxshall and Halsey, 2004; Wells,2007; Corgosinho and Martínez Arbizu, 2010; George, 2011;George and Müller, 2013). Damaged specimens were excludedfrom the analysis because it was impossible to identify them.

2.2. Environmental parameters

We examined the amount of CPE, which makes up the bulk ofintact chlorophyll a and its derivatives (phaeopigments), as anindicator of the amount of organic matter supplied to the sea floor.The ratio of the amount of chlorophyll a to the amount of phaeo-pigments (Chl a/phaeo) was used as an indicator of the freshnessof organic matter. The CPE samples were processed in the labora-tory according to the method of Greiser and Faubel (1988). Themean value of the three or four cores was regarded as the represen-tative value for each station.

We determined the MD and SC of sediments as parameters forthe distribution of grain sizes. The SC indicates the spread of thegrain size, with small SC indicating ‘well-sorted’ homogeneoussediment (Giere, 2009). The sediments were dispersed in boiled

Longitude Water depth (m) No. of cores investigated

128�05.010 E 430 4128�04.990 E 430 4128�21.480 E 1290 3126�51.810 E 1300 3126�53.970 E 1560 4126�54.020 E 1570 4126�42.110 E 1890 3128�30.020 E 1960 3128�42.980 E 3030 3127�02.930 E 3830 3129�06.860 E 3850 3127�25.050 E 4240 3129�06.620 E 5330 3130�20.000 E 4910 3129�50.020 E 5710 3129�39.380 E 6340 3127�20.880 E 7150 3

0 m

2000 m

4000 m

6000 m

8000 m

50° N

45° N

40° N

35° N

30° N

25° N

20° N120° E 125° E 130° E 135° E 140° E 145° E 150° E 155° E

100 km

PS01PS01

PS02PS02

PS03PS03

PS04PS04

PS05PS05

PS06PS06

PS07PS07

PS08PS08

RT01RT01

RT04RT04

RT03RT03

RT05RT05

RT1003RT1003RT1002RT1002

RT1004RT1004

126° E 127° E 128° E 129° E 130° E 131° E

27° N

26° N

25° N

24° N

Fig. 1. Sampling stations around the Ryukyu Trench. Labels indicate the names of each station (Table 1).

56 T. Kitahashi et al. / Progress in Oceanography 123 (2014) 54–63

water in a glass beaker and left for 24 h. Next, an ultrasonic vibra-tor was applied to the solution for 30–60 s. Then MD and SC weremeasured using a laser diffraction particle analyzer (CIRAS Co., Ltd.,1064 and SHIMADZU SALD-3000S). MD and SC data at stationsPS01–08, RT01 and RT03–05 were obtained from Itoh et al.(2011). It is worth considering that these values do not correspondto those of the sediment environment that meiofauna actuallyexperience, because the method used in this study may disinte-grate composite particles, such as fecal pellets in the sediment.These data are summarized in Table 2.

2.3. Harpacticoid diversity

The following diversity indices were used: the total number ofgenera identified at each station for genus richness (GR); the ex-pected number of genera for a theoretical sample of 15 specimens,estimated using the rarefaction method E(G15) (Hurlbert, 1971);the Shannon–Wiener diversity index (H0loge) for genus diversity;and the Shannon evenness measure or Pielou’s evenness (J0; Pielou,1975) for evenness of genera. For calculations of these indices, theactual numbers of each genus from each deployment were used.The stations at which fewer than 15 adults (PS01, RT01 andRT04) were identified were excluded from calculation of E(G15).

We calculated turnover diversity between geographical settings(b diversity) and between the Ryukyu and Kuril regions (regional

Table 2Environmental variables, harpacticoid density (adults and copepodids), number of adults

Station CPE (lg/cm2)

Chl a/phaeo

MD(lm)

SC Density (ind./10 cm2)

No. ofgenus

RT1004A 1.4 ± 0.2 1.7 ± 0.8 42.8 1.3 15.2 137RT1004C 0.9 ± 0.2 0.9 ± 0.8 37.1 1.4 15.1 138PS08 1.1 ± 0.7 2.7 ± 1.9 18.0 1.7 9.5 52RT1002 0.4 ± 0.1 1.2 ± 0.4 24.1 2.1 6.0 35RT1003B 0.3 ± 0.1 1.5 ± 0.8 10.5 1.3 4.4 28RT1003A 0.4 ± 0.2 1.8 ± 1.1 12.1 1.5 8.6 67RT05 0.4 ± 0.2 1.0 ± 1.0 1.5 2.3 5.6 27PS07 0.5 ± 0.3 2.2 ± 0.2 1.5 2.3 8.3 32PS06 0.3 ± 0.1 3.4 ± 3.4 2.1 2.3 4.9 19RT03 0.3 ± 0.1 2.1 ± 0.7 1.0 1.8 6.4 21PS05 0.5 ± 0.2 2.2 ± 0.7 1.3 1.8 4.1 16RT04 0.5 ± 0.2 1.4 ± 1.4 No

datumNodatum

2.9 7

PS04 0.3 ± 0.0 2.3 ± 2.0 2.5 2.1 4.9 18PS01 0.2 ± 0.0 2.1 ± 3.7 1.2 1.9 2.8 8PS02 0.3 ± 0.2 0.3 ± 0.5 1.2 1.8 3.8 15PS03 0.9 ± 0.6 2.2 ± 1.4 2.0 2.0 3.5 16RT01 0.7 ± 0.2 4.1 ± 2.6 No

datumNodatum

0.9 4

CPE data at stations PS01–08, RT01 and RT03–05 are cited from Kitahashi et al. (2012), anpigment equivalents; Chl a/phaeo, chlorophyll a/paeopigments; MD, median diameter oadults ident. to genus, the number of adult harpacticoids identified to the genus level; s

diversity, d diversity; Whittaker, 1972). Turnover diversity refersto the change in genus composition among settings (b diversity)and regions (d diversity). These measures were expressed as per-centages of dissimilarity and were calculated using the similaritypercentages (SIMPER) analyses (Clarke and Warwick, 2001), basedon a Bray-Curtis similarity matrix (see below; Gray, 2000).

2.4. Statistical analyses

As mentioned, animal diversity usually shows a unimodal trendwith increasing water depth. Some studies, however, have re-ported that diversity monotonically increases (e.g. Brault et al.,2013) or decreases with water depth (e.g. Trebukhova et al.,2013). Therefore, we adopted two models. We calculated both lin-ear and quadratic regressions for plots of each diversity indexagainst water depth and selected the model that showed a signif-icant relationship. If both models showed a significant relationship,the model was selected based on the Akaike’s information criterion(AIC; Akaike, 1973) (i.e. the model with a smaller AIC value wasselected).

The following multivariate methods were used to decipher theharpacticoid assemblages: non-metric multi-dimensional scaling(nMDS), permutational analysis of multivariate dispersions (PERM-DISP), permutational multivariate analysis of variance (PERMANO-VA), similarity percentages (SIMPER), distance-based linear models

identified to genus level and surveyed area at each station in the Ryukyu region.

adults ident. to No. of damagedspecimens

No. ofcopepodids

Core area analyzed(cm2)

4 180 211.23 177 211.28 90 158.46 54 158.41 63 211.26 108 211.21 60 158.47 93 158.43 55 158.42 79 158.45 44 158.40 39 158.4

7 52 158.40 30 158.44 41 158.45 30 145.20 11 158.4

d MD and SC data at these stations are cited from Itoh et al. (2011). CPE, chloroplasticf the sediment grain size; SC, sorting coefficient of the sediment grain size; no. of

urveyed area, the total area of sediments from which harpacticoids were extracted.

T. Kitahashi et al. / Progress in Oceanography 123 (2014) 54–63 57

(DISTLM) and the Mantel test. Prior to all analyses, density data(the mean densities of three or four cores for each genus) werelog10(x + 1)-transformed to reduce the contribution of abundantgenera and focus on the whole assemblage pattern. In this study,there were many zero values in the harpacticoid data set(Table S1). Therefore, the Bray–Curtis index was used as a similar-ity or dissimilarity index. This index excludes the effect of generathat are commonly absent from each of two samples (joint ab-sence) to avoid having the samples be considered more similar toone another due to many joint absences of genera (e.g. Andersonet al., 2011).

The nMDS can be used to visualize similarities in communitystructure across different stations. Using this method, stationsare plotted so that distances between plotted stations agree withmatching dissimilarities (Clarke and Warwick, 2001). The degreeto which the distances in the nMDS plot reflect the underlying dis-similarities was evaluated with the stress value (Clarke and War-wick, 2001).

PERMDISP was used to test for the homogeneity of dispersionsin genus compositions among topographical settings within theRyukyu region and among the Ryukyu and Kuril regions (Andersonet al., 2008).

PERMANOVA was used to test the null hypothesis that therewere no differences in community structure among different set-tings and among two regions by using the permutation method(Anderson et al., 2008). In addition, two-way crossed PERMANOVAwas used to detect the interaction between the factors ‘topograph-ical setting’ and ‘trench region’.

SIMPER analysis was used to determine the average of dissimi-larities in community structures between different topographicalsettings (b diversity) and different regions (d diversity). In addition,this analysis was used to compare community structures betweenthe same topographical settings in the two regions. To perform theanalysis, dissimilarities were computed between every pair of sta-tions in two different settings and regions, and the average of thedissimilarities was calculated (cf. Clarke and Warwick, 2001).

DISTLM was used to assess the effect of environmental factorson the changing patterns in the harpacticoid assemblage and topartition variation in the response data, using Euclidean distancesfor environmental indices and diversity indices. Although DISTLMdoes not make any explicit assumptions about the distribution ofexplanatory variables, in order to obtain more precise results fromthis model, the variables should not be heavily skewed (Andersonet al., 2008). Therefore, all environmental data were log-trans-formed before analysis (cf. Anderson et al., 2008). Stations RT01and RT04 were excluded from this analysis because the MD andSC values for these stations were not obtained (Itoh et al., 2011; Ta-ble 2). In DISTLM, one of two variables with a high correlation coef-ficient (|r| > 0.95) should be removed (cf. Anderson et al., 2008).Because the highest correlation coefficient (r = �0.72 for waterdepth and MD) was below this value, all environmental variables(water depth, CPE, Chl a/phaeo, MD and SC) were included in thisanalysis. The DISTLM procedure began with a null model contain-ing no predictor variables. First, the predictor variable with thebest value for the selection criterion (in this study, AIC) was se-lected, followed by the variable that, together with the first one,most improved the selection criterion (Anderson et al., 2008).The procedure stopped when no further improvement was possi-ble in the selection criterion. At each step of the procedure, a con-ditional test was used to determine whether adding a particularvariable contributed significantly to the explained variation(Anderson et al., 2008). For each test, 9999 permutations wereperformed.

The Mantel test was used to test whether the two dissimilaritymatrices were significantly correlated (Sokal and Rohlf, 1995; Bor-card et al., 2011). This test was used to assess the significance of

the relationship between harpacticoid community structure andwater depth. The Mantel test was conducted with R (R Develop-ment Core Team, 2008) by using the package vegan (Oksanenet al., 2008). Other multivariate analyses were performed usingPRIMER6 software with PERMANOVA+, an add-on package (PRI-MER-E Ltd., Plymouth, UK).

3. Results

A total of 1908 harpacticoid copepods were collected. Of these,640 adults were identified to the genus level, yielding 97 generabelonging to 22 families (Tables 1 and S1). The most abundant gen-era were Pseudobradya Sars, 1904 (14.0%), Zosime Boeck, 1872(9.7%), Pseudomesochra T. Scott, 1902 (8.0%), Marsteinia Drzycimski,1968 (5.1%), Bradya Boeck, 1872 (4.9%), and Halectinosoma Lang,1944 (4.5%). No harpacticoid specimens were found in the residualsediments at stations where the Ludox method was used to extractmeiofauna (RT1002–1004). Escobar-Briones et al. (2008) reportedsignificant differences in the meiofaunal density and compositionwhen manual vs. centrifuge sorting was used. It would not beneeded to concern about the difference in extraction efficiency ofthe two method used in the present study.

3.1. Bathymetric patterns in harpacticoid diversity in the Ryukyuregion

Water depth, environment variables and density of harpactic-oids (adults and copepodids) are shown in Table 2. The mediandiameter of sediment grains (MD) was negatively correlated withwater depth (r = �0.72, p < 0.01), but other environmental param-eters were not significantly correlated with water depth. The den-sity of harpacticoids (adults and copepodids) significantlydecreased with increasing water depth (r = �0.84, p < 0.001).

The genus richness (GR) and the Shannon–Wiener index(H0loge) significantly decreased with increasing water depth (GR:32–4; H0loge: 2.82–1.39; Fig. 2a and c; Table 3). No significant rela-tionship was detected between the expected number of genera,E(G15), and water depth for the linear and quadratic models(Fig. 2b, Table 3). Evenness (J0) increased with water depth (0.80–1.00) and slightly decreased at hadal depths (Fig. 2d, Table 3). J0

was significantly correlated with water depth, as revealed by thelinear (p < 0.01) and quadratic (p < 0.01) models; however, theAIC value of the quadratic model was smaller than that of the lin-ear model and thus a better fit (quadratic: AIC = �59.6; linear:AIC = �53.0).

DISTLM analysis successfully detected the environmental vari-ables that significantly explained the differences in diversity indi-ces (Table 4). The differences in GR were significantly explainedby water depth (71%). The values for SC and Chl a/phaeo explainedthe significant differences in E(G15) for 40% and 23% of the differ-ences, respectively. DISTLM analysis selected water depth andChl a/phaeo as predictors of the differences in H0loge, and waterdepth alone significantly explained 36% of the variation. The differ-ence in J0 was significantly explained by water depth (67%).

3.2. Spatial pattern in harpacticoid community structure in the Ryukyuregion

For each topographical setting, the 10 most abundant generaare shown in Table 5. The most dominant genera were Pseudobra-dya (24%), Pseudobradya (10%), Marsteinia (11%), Bradya (17%) andPseudozosime (17%) in the bathyal zone, on the upper trench slope,on the lower trench slope, on the trench floor and on the abyssalplain, respectively.

1000 2000 3000 4000 5000 6000 7000

5

10

15

20

25

30

Water depth (m)

GR

1000 2000 3000 4000 5000 6000 7000

4

6

8

10

12

Water depth (m)

1000 2000 3000 4000 5000 6000 7000

1.5

2.0

2.5

3.0

Water depth (m)

H'lo

ge

1000 2000 3000 4000 5000 6000 7000

0.80

0.85

0.90

0.95

1.00

Water depth (m)

E (G

15)

J'

ba

dc

Fig. 2. Bathymetric patterns of harpacticoid diversity in the Ryukyu region: (a) the number of genera, GR; (b) the expected number of genera, E(G15); (c) the Shannon–Wienerindex, H0loge; and (d) evenness, J0 . Open circles indicate the stations where fewer than 15 adults were identified.

Table 3Values of diversity indices at each station in the Ryukyu region.

Station GR E(G15) H0loge J0

RT1004A 32 9.53 2.82 0.81RT1004C 28 8.92 2.65 0.80PS08 25 11.49 3.00 0.93RT1002 22 11.54 2.86 0.92RT1003B 15 10.46 2.55 0.94RT1003A 33 11.71 3.19 0.91RT05 18 11.95 2.78 0.96PS07 22 12.76 3.02 0.98PS06 13 11.00 2.43 0.95RT03 15 11.84 2.62 0.97PS05 11 10.50 2.27 0.94RT04 7 * 1.95 1.00PS04 14 12.25 2.58 0.98PS01 8 * 2.08 1.00PS02 9 9.00 2.03 0.92PS03 13 12.31 2.45 0.96RT01 4 * 1.39 1.00

GR, the number of genera at each station; E(G15), the expected number of genera;H0loge, the Shannon–Wiener diversity; J0 , evenness.* Stations where fewer than 15 adults were identified.

Table 4Results of DISTLM analyses on diversity indices and community structure ofharpacticoids in the Ryukyu region.

Variable Pseudo-F p Var (%) Cumul (%)

GR+Depth 32.5 <0.001 71.4 71.4

E(G15)+SC 8.0 <0.05 40.0 40.0+Chl a/phaeo 6.9 <0.05 23.1 63.1

H0loge+Depth 7.1 <0.05 35.5 35.5+Chl a/phaeo 2.4 n.s. 10.9 46.4

J0

+Depth 26.1 <0.001 66.7 66.7+Chl a/phaeo 3.4 n.s. 7.4 74.1+CPE 3.7 n.s. 6.5 80.6+SC 2.6 n.s. 4.0 84.6

Community structure+Depth 3.3 <0.001 20.2 20.2

n.s., Not significant; Var, the proportion of explained variation attributable to eachvariable; Cumul, cumulative total proportion of explained variation. Plus signs (+)indicate the variables added to the explained variation.

58 T. Kitahashi et al. / Progress in Oceanography 123 (2014) 54–63

The structure of harpacticoid communities was highly dissimi-lar in different settings (70–82%, Fig. 3). In addition, a significantdifference in dispersions was detected between topographical set-tings (PERMDISP, F = 15.4, p < 0.05) and a significant difference wasdetected across different topographical settings in the Ryukyu re-gion (PERMANOVA, pseudo-F = 1.79, p < 0.01). DISTLM detectedthat the difference in harpacticoid assemblage was significantlyexplained by water depth (20%, Table 4).

3.3. Comparison with the Kuril region

In the Kuril region, Kitahashi et al. (2013) obtained data on 79genera in 18 families (Table S2), including 56 genera that also werefound in the Ryukyu region. The comparison of genus compositionsin the Ryukyu and Kuril (Kitahashi et al., 2013) regions (nMDS) isshown in Fig. 4. The stress value was sufficiently low (0.18), indi-cating that the nMDS plot obtained in this study was a useful

Table 5List of harpacticoid genera collected at each topographical setting and their relative densities in the Ryukyu region.

Bathyal Upper trench slope Lower trench slope Trench floor Abyssal plain

Genus % Genus % Genus % Genus % Genus %

Pseudobradya 23.6 Pseudobradya 10.1 Marsteinia 11.1 Bradya 17.2 Pseudozosime 17.4Zosime 16.0 Pseudomeaochra 8.7 Pseudomesochra 9.9 Pseudomesochra 10.9 Marsteinia 13.0Halectinosoma 8.0 Zosime 6.4 Zosime 7.4 Pseudobradya 9.4 Mesocletodes 8.7Pseudomesochra 6.5 Bradya 6.1 Bradya 6.2 Marsteinia 9.4 Bradya 8.7Pseudameira 5.1 Marsteinia 6.1 Sarsameira 4.9 Pseudozosime 9.4 Parameiopsis 4.3Stylicletodes 5.1 Pseudozosime 3.6 Pseudobradya 4.9 Halectinosoma 6.3 Fultonia 4.3Delavalia 3.3 Pseudameira 3.5 Eurycletodes 3.7 Nitocra 4.7 Neoargestes 4.3Ameira 2.9 Ameira 2.9 Mesocletodes 3.7 Parameiopsis 4.7 Canuellina 4.3Sarsameira 2.5 Halectinosoma 2.6 Nematovorax 3.7 Sarsameira 4.7 Nannopodella 4.3Bryocamptus 2.5 Stylicletodes 2.5 Pseudozosime 3.7 Eurycletodes 4.7 Monocletodes 4.3

Neoargestes 4.7 Nematovorax 4.3Odiliacletodes 4.7 Emertonia, 4.3Microsetella 4.7 cf. Huys (2009)Tisbisoma 4.7 Meiopsyllus 4.3

Dactylopodella 4.3Paradanielssenia 4.3Pseudomesochra 4.3

Only the top 10 genera are shown, unless the percentages were tied.%, percentage of the total number of harpacticoid adults identified to the genus level in the samples fromgiven topographical settings.

Trench floorTrench floor

Abyssal plainAbyssal plain

Lower trench slopeLower trench slope

Upper trench slopeUpper trench slope

BathyalBathyal

82%75%

70%

71%

Fig. 3. Dissimilarity values in harpacticoid community structures between topo-graphical settings in the Ryukyu region.

T. Kitahashi et al. / Progress in Oceanography 123 (2014) 54–63 59

summary of the station relationships (Clarke and Warwick, 2001).The nMDS plot showed that the difference in the harpacticoid com-position between the two regions (Fig. 4). Moreover, the difference

Bray-Curtis similarityStress: 0.18

Fig. 4. The nMDS ordination based on the genus composition in the Ryukyu and Kurilsymbols indicate the stations in the Kuril region (Kitahashi et al., 2013). (For interpretatversion of this article.)

was statistically significant (PERMANOVA, pseudo-F = 2.89,p < 0.005), whereas no significant difference in dispersions was de-tected between the two trench regions (PERMDISP, F = 0.37,p > 0.05).

Genus composition and water depth were significantly corre-lated in the Ryukyu region (Mantel test, r = 0.34, p < 0.05) and inthe Kuril region (Kitahashi et al., 2013). Community structuresaround the shallow stations were quite similar to each other, butthey became more distinct as water depth increased (Fig. 4). Com-munity structures were compared between the same topographi-cal settings in the two regions using SIMPER analysis (Fig. 5). Theaverage dissimilarity value between the Ryukyu and Kuril regionswas 79%. Specifically, the average dissimilarity values between thebathyal zones, upper trench slopes, lower trench slopes, trenchfloors and abyssal plains were 62%, 72%, 78%, 88% and 91%, respec-tively. In addition, a significant interaction between the factors‘topographical setting’ and ‘trench region’ was detected (two-wayPERMANOVA, pseudo-F = 1.65, p < 0.01).

BathyalUpper trench slopeLower trench slopeTrench floorAbyssal plain

regions. Red symbols indicate the stations in the Ryukyu region (this study). Blueion of the references to color in this figure legend, the reader is referred to the web

Kuril region Ryukyu region78.7%

61.7%

71.7%

77.7%

87.9%

90.7%

Bathyal

Trench floor

Abyssal plain

Upper trench slope

Lower trench slope

Bathyal

Trench floor

Abyssal plain

Upper trench slope

Lower trench slope

Fig. 5. Dissimilarity values between the Ryukyu and Kuril regions.

60 T. Kitahashi et al. / Progress in Oceanography 123 (2014) 54–63

4. Discussion

4.1. Bathymetric patterns in environmental variables and harpacticoiddiversity around trenches

Harpacticoid density (adults and copepodids) significantly de-creased with increasing water depth, whereas CPE was not corre-lated with water depth around the Ryukyu Trench (Table 2).

Many studies have reported that benthic diversity increaseswith water depth down to 2000–3000 m, after which it declinesagain (e.g. Rex, 1981). The diversity–productivity theory might ex-plain the unimodal pattern of biodiversity (Rex and Etter, 2010).This theory rests on the fact that organic matter flux decreaseswith increasing water depth (Rex and Etter, 2010). In shallower re-gions, where high organic matter flux leads to high populationdensities, strong biological interactions depress diversity. In con-trast, in deeper regions, organic matter is scarce, and animal den-sity is too low to sustain reproductively viable populations (Alleeeffect; Rex, 1973), leading to low diversity. Thus, diversity is higherat an intermediate depth than in shallower and deeper regions.

In the Ryukyu region, diversity indices (GR and H0loge) of harp-acticoid copepods also significantly decreased with water depthalthough few adult harpacticoids were found in this region, espe-cially at deeper stations (PS01, RT01 and RT04; Table 2). Further-more, data from these stations were excluded in the rarefactionmethod, which obscured the relationship between water depthand E(G15). The DISTLM revealed that two aspects of harpacticoiddiversity (E(G15) and H0loge) were correlated with water depth orthe quality of organic matter (Chl a/phaeo) in the Ryukyu region(Table 4), and these indices increased with increasing Chl a/phaeo(Table 2). These results indicate that only the deeper side of theunimodal pattern between diversity and water depth appears inthe Ryukyu region, due to low surface productivity (cf. Berger,1989; NASA SeaWiFS Project).

Previous studies have proposed that a peak or subsequentdescending phase of the productivity–diversity relationship maynot exist in deep-sea environments, where food availability is lim-ited (Rose et al., 2005; George et al., 2013). As mentioned, harpac-ticoid diversity increased with the increasing food availability(especially food quality) in the Ryukyu region. In contrast, in theKuril region, harpacticoid diversity displayed a unimodal patternwith water depth, with peaks appearing at intermediate depths.In this region, diversity decreased as food quality increased (Kitah-ashi et al., 2013). Contrary to the pattern in the Ryukyu region, foodavailability would be so high that the diversity decrease due tohigh food availability in this region. These facts indicate that thebathymetric pattern of diversity differs depending on the level ofsurface productivity, although other factors, such as temperatureand sediment heterogeneity, might affect the bathymetric patternof diversity.

The evenness of harpacticoid genera evaluated by J0 increasedwith water depth (Fig. 2d). A slight decrease in the evenness of

genera at the hadal depths resulted from the low number of iden-tified specimens at hadal stations (Table 2). Meanwhile, low even-ness at shallow depths might be due to extensive hydrodynamicdisturbances, resulting in high dominance of specific genera (Gageet al., 2000). Alternatively, the grain size distribution could affectthe bathymetric pattern in the evenness. Tietjen (1984) suggestedthat heterogeneous sediments provide more microhabitats andharbor high levels of diversity and evenness. This relationship be-tween sediment heterogeneity and nematode evenness were re-ported from the Puerto Rico Trench (Tietjen, 1989) and theAtacama Trench (Gambi et al., 2003). The significant and positiverelationship was detected between SC and J0 in the present study(Table 3). Therefore, the heterogeneity of sediment is believed toaffect the evenness of harpacticoid genera around the RyukyuTrench.

4.2. b Diversity in the Ryukyu region

Among nematodes, low similarity at the genus and species lev-els has been reported in community comparisons between thetrench floor and the adjacent slope stations (1000–4000 m) inthe Puerto Rico Trench (Tietjen, 1989), Atacama Trench (Gambiet al., 2003) and South Sandwich Trench (Vanhove et al., 2004).However, these studies compared only hadal and shallow assem-blages and did not examine the gradual changes that occur overincreasing water depth. In the case of harpacticoid assemblagesin the Kuril region, harpacticoid community structure showedgradual changes as water depth increased from the bathyal to ha-dal depth (Fig. 4; Kitahashi et al., 2013). This pattern also appearedin the Ryukyu region (Fig. 4). A shift in harpacticoid assemblageshas been reported at bathyal and abyssal depths (e.g. Coull,1972; Hicks and Coull, 1983; Shimanaga et al., 2008). To ourknowledge, the present study is one of the first to detect the depthgradients of community structure for harpacticoid copepods frombathyal to hadal depths.

In the Atacama Trench, differences in nematode communitystructure between hadal and shallow stations were attributed tothe presence or absence of certain genera (Gambi et al., 2003),whereas in the Puerto Rico Trench (Tietjen, 1989) and South Sand-wich Trench (Vanhove et al., 2004), differences were thought to re-sult from differences in the relative abundance of each nematodegenus. During our study, changes in the relative abundance of eachharpacticoid genera were found. For example, the genus Pseudobr-adya dominated in the shallow stations and its dominance de-creased as water depth increased, whereas the genus Bradyaincreased its dominance as water depth increased (Tables 5 andS1). These changes in the relative abundance of genera with waterdepth indicate a gradual change in the community structure of har-pacticoids in the Ryukyu region.

PERMDISP analysis detected heterogeneity in multivariate dis-persion between the topographical settings in the Ryukyu region.In addition, dispersions of stations on nMDS plot became large aswater depth increased (Fig. 4). These results indicate that the com-munity structure of harpacticoids at the scale of kilometer be-comes heterogeneous with increasing water depth andhomogeneous in shallow depths. This finding suggests that dis-persal by means of bottom water currents (e.g. Thistle, 1988; Bagu-ley et al., 2006) and ‘emergence’ behavior (excursion into the watercolumn to escape from unsuitable conditions or predation, Thistleet al., 2007) occur more actively at shallow depths than at deeperdepths.

PERMDISP analysis detected heterogeneity in multivariate dis-persion between the topographical settings in the Ryukyu region.In fact, the dispersions in harpacticoid composition differed be-tween the settings (Fig. 4). However, at the same time, nMDS plotshowed the stations from the different settings separated from

T. Kitahashi et al. / Progress in Oceanography 123 (2014) 54–63 61

each other (Fig. 4). Moreover, PERMANOVA analysis revealed sig-nificant differences in community structure between the settingsin the Ryukyu region. These results suggest that the communitystructure of harpacticoids differed between settings among theRyukyu region. The dissimilarity values were equally high betweenall depth zones in the Ryukyu region (Fig. 3), whereas in the Kurilregion, the values between the trench floor and either the lowertrench slope or abyssal plain stations were much larger than thosebetween the three slope zones (Kitahashi et al., 2013).

In the present study, the DISTLM analysis found that waterdepth was the variable that best explained the variation in thecommunity structure of harpacticoids in the Ryukyu region (Ta-ble 4). Nevertheless, water depth itself is unlikely to affect harp-acticoid assemblages. Therefore, it seems that the harpacticoidcommunity structure is certain factors associated with waterdepth, in both the Ryukyu and Kuril regions (Kitahashi et al.,2013). However, the majority of the total variation was not ex-plained by the factors in the analyses in either region. Therefore,a factor that was not examined in this study, such as interactionwith other meiofaunal and macrofaunal organisms (e.g. Patersonand Lambshead, 1995), must affect the harpacticoidcommunities.

4.3. d Diversity between the two trench regions

In the present study, there was high d diversity (79%) at thegenus level between the Ryukyu and Kuril regions (2000 km apartfrom each other; Fig. 5). This result is not surprising because thetwo regions belong to different geographical provinces, as recentlyproposed by Watling et al. (2013). Similar values of d diversity atthe species level have been reported: 72–78% between nematodeassemblages in the eastern and western basins of the Mediterra-nean (1000 km apart, Danovaro et al., 2008) and 82% betweennematode assemblages from the Portuguese and the Catalan mar-gins (1100 km apart, Danovaro et al., 2009). Dissimilarity values atthe genus level obtained in this study were less than or equal tothose reported at the species level. Therefore, the dissimilarity va-lue obtained in this study is a conservative estimate. However, thedissimilarity in community structures between the two regionswas as high as the dissimilarities among the different settingswithin each region. This finding suggests that the differences inenvironmental conditions within regions have a comparable im-pact on the harpacticoid assemblages within regions, although pri-mary production and other factors in the euphotic zone differbetween the two regions.

There was a bathymetric change in d diversity between the Ryu-kyu region (as found in this study) and the Kuril region (Kitahashiet al., 2013). The harpacticoid community structures between thetwo regions were similar at the shallow depths, but the dissimilar-ity between those regions became more striking as water depth in-creased (Figs. 4 and 5). In addition, the result of two-wayPERMANOVA suggested that the changing pattern of communitystructure among geographical settings was dependent on thetrench region. This discrepancy in the pattern may reflect the dif-ferences in the level of primary productivity.

Alternatively, the isolation of assemblages on trench floors andabyssal plains between two regions may be attributed to a physicalbarrier such as the Izu-Ogasawara Arc and Trench, which are lo-cated between the two regions and may prevent the expansionof harpacticoid distribution ranges (Kitahashi et al., 2012). Manybenthic animals that inhabit the abyssal plains never experiencesubstantial variations in water depth (i.e. water pressure) (Jamie-son et al., 2010); therefore, exchange among regions may be diffi-cult for deep-sea benthic animals, including harpacticoidcopepods.

5. Conclusion

Food availability drastically changes around trenches, whichmakes the trench region a suitable area in which to assess the rela-tionship between biodiversity and environment. We investigatedthe diversity of harpacticoid copepods around the Ryukyu Trenchand compared it with the diversity found around the Kuril Trench(Kitahashi et al., 2013). Our results indicate that the bathymetricpattern of a diversity depends on the level of primary productionin the euphotic zones. We also showed that the community struc-ture of harpacticoids gradually changes with water depth in bothregions, in spite of the great difference in primary productivity lev-els. However, d diversity between the two regions increases alongwith water depth. These findings suggest that the bathymetric pat-terns of harpacticoid assemblages differ among regions and thatthese discrepancies reflect differences in environmental condi-tions, such as primary productivity.

Acknowledgments

We thank the officers and crew of the research vessels HakuhoMaru and Tansei Maru and the supporting staff of the Japan Agencyfor Marine–Earth Science and Technology (JAMSTEC). We alsothank Mr. Ayanori Misawa, who provided the hydrographic chart(Fig. 1). Generic Mapping Tools (GMT, Wessel and Smith, 1995)was used in this study. We would like to thank the three anony-mous reviewers who provided helpful comments on an earlierdraft of the manuscript. This study was partly supported by a Grantfrom the Ministry of Education, Sports, Culture, Science, and Tech-nology of Japan (No. 22770022).

Appendix A. Supplementary material

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.pocean.2014.02.007.

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