Species diversity and vertical distribution of the deep-sea copepods of the genus Euaugaptilus in the Sulu and Celebes Seas

Deep-Sea Research II 57 (2010) 2098–2109

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Species diversity and vertical distribution of the deep-sea copepods of the genus Euaugaptilus in the Sulu and Celebes Seas Hiroyuki Matsuura 1, Shuhei Nishida n, Jun Nishikawa Atmosphere and Ocean Research Institute, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa 277-8564, Japan

a r t i c l e in f o

a b s t r a c t

Available online 21 September 2010

The relationships between water-column structure, species diversity and patterns of vertical distribution were examined in the copepod genus Euaugaptilus in the Sulu and Celebes Seas. Euaugaptilus is among the most species-rich single genus of all calanoid copepods and is characterized by the specialized ‘button setae’ in their mouth appendages. The Sulu Sea is a semi-enclosed equatorial basin located in the center of the Indo-Malayan Archipelago, rimmed by sills shallower than 420 m, and characterized by homogeneous, warm water (ca. 10 1C) from the mesopelagic zone to the sea bottom of ca. 5000 m, while the adjacent Celebes Sea is of more typical oceanic conditions. Plankton samples were collected at two stations both day and night from 16 discrete layers in the upper 1000 m. A total of 29 species of Euaugaptilus were collected in the Celebes Sea, which is among the largest numbers for the genus so far reported from a single restricted sea area, but only 8 species were collected in the Sulu Sea. These 8 species occurred in the upper mesopelagic zone in the Celebes Sea, while in the Sulu Sea many of them extended their ranges and/or shifted into deeper zones. An additional 15 net tows to depths deeper than 1000 m added 6 species from the Celebes Sea and 8 species from the Sulu Sea, with all the deep Sulu species, except E. hyperboreus, being found above 1000 m in the Celebes Sea. This drastic reduction of species number in the Sulu Sea is attributed to the homogenous high-temperature deep water, which may have prevented settlement of many deep-water species from outside areas and co-existence of species sharing similar ecological niches. The species in the Sulu Sea showed discrete vertical distribution patterns according to the species or species groups, despite the essential absence of vertical gradients of temperature and salinity in the mesopelagic zone. The species pairs that showed similar vertical distributions in the Sulu Sea showed marked differences in their prosome length and/or in the morphology of the ‘button setae’ and the mandible blade. The species successfully inhabiting the Sulu Sea may have expanded their range into the deep waters, and vertical segregation and food-resource partitioning may be among the major factors allowing the observed coexistence of these congeneric species. & 2010 Elsevier Ltd. All rights reserved.

Keywords: Copepods Euaugaptilus Mesopelagic zone Vertical segregation Feeding guild Resource partitioning

1. Introduction Oceanic zooplankton communities are characterized by the co-occurrence of many species in particular water masses or geographic regions (see Angel, 1993, for review), and the mechanism for their coexistence has been a major concern in zooplankton ecology. There are previous studies that specifically addressed these topics, e.g., on feeding behavior of copepods in relation to niche separation (Mullin, 1966), spatio-temporal patterns of copepods in dominance and diversity (McGowan and Walker, 1985), vertical habitat segregation of copepods in the thermally stratified water of

n

Corresponding author. E-mail address: [email protected] (S. Nishida). 1 Present address: Department of Fisheries, School of Marine Science and Technology, Tokai University, 3-20-1 Orido, Shimizu, Shizuoka 424-8610, Japan. 0967-0645/$ - see front matter & 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2010.09.013

the eastern tropical Pacific (Longhurst, 1985), vertical habitatpartitioning in oceanic copepods (Ambler and Miller, 1987), and on patterns of coexistence in congeneric copepods (Peralba and Mazzocchi, 2004). These studies dealt mainly with epipelagic and/or coastal assemblages and focused on relatively abundant species. Accordingly, little is known of the oceanic, mesopelagic assemblages, in which the highest species diversity has been observed in many taxa and regions, encompassing many non-dominant species (Angel, 1993; Mauchline, 1998). Recently, Kuriyama and Nishida (2006) examined the vertical distribution of the scolecitrichid copepods in Sagami Bay, central Japan, and proposed that the highly diverse assemblage of these copepods may be structured, for the major part, through vertical partitioning of habitats and partitioning of food resources. Wishner et al. (2008) examined the vertical distributions of calanoid copepods in the oxygen minimum zone of the Arabian Sea (300-1000 m), analyzed spatio-temporal differences of copepod distribution in relation to environmental features, and found

H. Matsuura et al. / Deep-Sea Research II 57 (2010) 2098–2109

considerable distributional and ecological changes associated with very small oxygen gradients. The genus Euaugaptilus is among the most species-rich genera of oceanic copepods, next to Paraeuchaeta, encompassing ca. 73 described species (Boxshall and Halsey, 2004). They are essentially inhabitants of the meso- and bathypelagic zones of the oceans wherein many congeneric species occur sympatrically (e.g. Grice and Hulsemann, 1965; Roe, 1972; Deevey and Brooks, 1977). The genus is also characterized by the structure of their mouth appendages that have ‘button setae’ furnished with rows of sucker-like elements which are assumed to function in the capture of food organisms (Boxshall, 1985; Matsuura and Nishida, 2000). For these reasons the genus Euaugaptilus would be an interesting model group for examining the species diversity and the mechanisms of coexistence of congeneric species in the same feeding guild (specialized carnivory) in the meso- and bathypelagic zones of the oceans. The Sulu Sea is a semi-enclosed marginal sea in the western equatorial Pacific, surrounded by islands and sills mostly shallower than 200 m (Exon et al., 1981), with a single 420 m deep channel in the Mindoro Strait. The basin is characterized by homogeneous warm water (ca. 10 1C) from the mesopelagic zone to the sea bottom of ca. 5000 m (Frische and Quadfasel, 1990) with similarly constant salinity and dissolved oxygen. While the Sulu Sea exhibits such characteristic hydrographic features, the adjacent Celebes Sea is of more typical open-ocean conditions with the water temperature decreasing with depth to ca. 3.8 1C at 5000 m (Wyrtki, 1961; Nishida and Gamo, 2004). Thus these areas together provide an excellent setting to examine the responses in vertical distribution patterns and species diversity profiles of zooplankton in areas of different water-column structure. However, little information was available concerning the distribution of zooplankton in these areas until recently. On the basis of the cruises of the RV Hakuho Maru in 2000 and 2002 (Nishida and Gamo, 2007), Nishikawa et al. (2007) demonstrated that the warm and homogeneous mesopelagic water (o1000 m) in the Sulu Sea does not greatly influence the total mesozooplankton standing stock, vertical distribution patterns or the community structure at the higher taxonomic levels compared with adjacent seas, while marked differences were noted in the composition of copepod families between the Sulu and Celebes Seas. Chaetognath species also showed marked differences in species diversity and vertical distributions (Johnson et al., 2006). These studies suggest possible differences in vertical distribution patterns and diversity profiles of zooplankton at lower taxonomic levels (genera and/or species) in these seas. The present study examines the vertical distribution of copepods of the family Augaptilidae in the Sulu and Celebes Seas, with particular reference to the patterns of species diversity of the genus Euaugaptilus and the effect of warm mesopelagic water in the Sulu Sea on the vertical patterns of congeneric copepods.

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Possible resource partitioning among the species is also discussed with reference to the functional morphology of the copepods’ feeding appendages. This is part of a study on the zooplankton community in the Sulu Sea and adjacent waters, of which the vertical distributions of higher taxonomic groups has been reported by Nishikawa et al. (2007), and those of chaetognaths by Johnson et al. (2006), while the species diversity and vertical distribution of the copepod communities in general will be addressed elsewhere.

2. Materials and methods 2.1. Sampling and sample processing Zooplankton were collected using a MOCNESS-1 (Multiple Opening-Closing Net and Environmental Sensing System; effective mouth area during operation, 1 m2; mesh size, 0.33 mm: Wiebe et al., 1976) at stations in the Celebes (Stn 23) and Sulu Seas (Stn 26) during a cruise KH-00-1 of the R/V Hakuho Maru in February 2000 as described in Nishikawa et al. (2007). At each station samples were collected from 16 discrete depth layers in the upper 1000 m both day and night. The sequence of depth intervals was every 25 m from 0 to 200 m and every 100 m from 200 to 1000 m (Table 1). The volume of water filtered in each layer ranged between 220-560 m3 (median: 370 m3) and 790-1330 m3 (median: 1100 m3) in the shallow and deep tows, respectively. Additional samples were collected at a total of 15 stations during the same cruise and another cruise (KH-02-4) in November-December 2002 using an ORI net (Omori, 1965; mouth diameter, 160 cm; mesh size, 0.33 mm or 0.69 mm) or a 10-ft Isaacs-Kidd mid-water trawl (IKMT: Isaacs and Kidd, 1953; mesh size, 1.0 mm) which covered the layers deeper than 1000 m down to ca. 2300 m (Fig. 1, Table 2). The depths reached by the latter 2 nets were monitored with a digital depth meter (RMD-2000: Rigosha Co. Ltd.), or estimated from the lengths and angles of the wire where the wire was paid out more than 3600 m. The volume of water filtered ranged between 4260-9000 m3 (median: 5750 m3) in the ORI net and 12,550-167,000 m3 (median: 41,550 m3) in the IKMT. The samples were immediately fixed and preserved in 4% formaldehyde/ seawater solution buffered with sodium tetraborate. At each MOCNESS station, water temperature and salinity were measured with a CTD-system separate from the net (SBE 9 plus with SBE 32 Carousel water sampler, SEA-BIRD Electronics, INC.) and dissolved oxygen was measured with an automatic Winkler’s titrating machine (Hirama ART-3) (Nishimura and Ohwada, 2003). The adults and immature copepodids of the family Augaptilidae were sorted from the original samples, identified to genus, and numbers enumerated. The copepods of the genus Euaugaptilus were

Table 1 Sampling records for the MOCNESS in the Celebes and Sulu Seas. Cruise

KH-00-1

Area

Stn.

Celebes

23

Sulu

26

Time: D, Day; N, Night.

Date

19 19 19 20 24 25 25 25

Feb Feb Feb Feb Feb Feb Feb Feb

Time

2000 2000 2000 2000 2000 2000 2000 2000

D D N N N N D D

Sampling depth

Bottom

Geographic position

(m)

depth (m)

Latitude (N)

200–1000 0–200 200–1000 0–200 200–1000 0–200 200–1000 0–200

5388 5398 5397 5376 4890 4887 4889 4878

21 21 21 21 71 71 71 71

25.80 25.10 28.30 31.70 33.70 33.30 38.00 33.50

Longitude (E) 1221 1221 1221 1221 1211 1211 1211 1211

28.20 28.10 28.80 30.00 29.10 28.20 29.40 25.90

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to the following equation:

further identified to species after Park (1993), Bradford-Grieve (1999), and references therein for both the adults and immature copepodid stages and their respective numbers enumerated. All samples were examined in their entirety. The copepod abundance was expressed in values per 1000 m3 of water filtered or in values per m2 of 0-1000 m water column. For the Euaugaptilus species that occurred in the Sulu Sea, the prosome length (PL) of adult females was measured and the structure of mouthpart appendages was examined by light and scanning electron microscopy (SEM) after Matsuura and Nishida (2000).

Hu ¼ Spi ln pi , where the pi is the proportion of individuals found in the ith species. For the description of vertical distribution, the depth (Dx%) above and below which x% of the population resided was calculated for each species (Pennak, 1943). The community structure of Euaugaptilus between the sampling layers at both stations was compared using the Bray-Curtis similarity index based on the log10(x+1)-transformed abundance data of species. Hierarchical clustering with group-average linking based on sample similarities was performed. All analyses were performed with the software package PRIMER v6 (Plymouth Marine Laboratory).

2.2. Data processing For comparison of species diversity between the sampling layers, in addition to the total species numbers from the original samples (S), the Shannon-Wiener index was calculated according

3. Results 3.1. Hydrography The hydrographic conditions at the MOCNESS stations are shown in Fig. 2 (see also Nishikawa et al., 2007). While the surface mixed layer of high-temperature ( 4271C) and the steep thermocline (75-200 m, 27-15 1C) was common in both seas, the temperature decreased more gradually in the Sulu Sea and was ca.10 1C from 600 m to 1000 m (Fig. 2B) in contrast to the Celebes Sea where temperature continued to decrease to 4.6 1C at 1000 m (Fig. 2A). In the Sulu Sea the salinity increased from the surface (34.0) to 200 m (34.5) and was nearly constant at ca. 34.4-34.5 from 400 to 1000 m (Fig. 2B), while in the Celebes Sea there was a steep halocline from the surface (33.4) to the subsurface maximum (34.7) in 100-200 m, followed by a minimum at 200-300 m (Fig. 2A). The dissolved oxygen content in the Sulu Sea sharply decreased from the near-surface ( 43 ml l  1) to ca. 100 m (ca. 2.0 ml l  1), followed by a more gradual decrease to 400 m and constant values of ca. 1.5 ml l  1 between 400-1000 m (Fig. 2B). In the Celebes Sea the water in the upper 300 m was more oxygenated ( 42 ml l  1) than in the Sulu Sea and there was an oxycline from 200 m to the minimum of ca.1.6 ml l  1 at 500 m followed by a gradual increase to ca.1.8 ml l  1 at 1000 m (Fig. 2A).

Fig. 1. Location of sampling stations. Filled circles and/or italic numerals indicate stations for day/night series of MOCNESS, and open circles and/or roman numerals those for oblique tows of ORI net and/or IKMT.

Table 2 Occurrence of species of the genus Euaugaptilus in the Celebes and Sulu Sea from IKMT and ORI-net tows that reached below 1000 m. Only those species that were not collected by the 0-1000 m MOCNESS tows are shown. Sea area

Sulu Sea

Celebes Sea

Cruise Station Net* Depth reached (m)**

00-1 26 IK 1444

02-4 4-1 IK 1300

02-4 4-2 ORI 1872

02-4 4-3 IK 2300

02-4 6 IK 1300

02-4 10 IK 1300

02-4 11 IK 2300

02-4 12 IK 1300

02-4 13 IK 1200

00-1 22 IK 1333

00-1 23 IK 1033

02-4 2-1 IK 1666

02-4 2-2 IK 1666

02-4 3-1 ORI 1299

02-4 3-2 IK 1666

Species E. hyperboreus E. laticeps E. latifrons E. longimanus E. magnus E. oblongs E. perodiosus E. rigidus E. austranus E. clavatus E. fecundus E. indicus E. matsuei

+            

++     + + +     

++            

+++ +   +  +++      

     +       

   +    +     

+   +   ++      

+       +     

+  +   + +      

+          +  +

++          + + 

+        +   + +

+          + + 

           + +

        + + +  

Symbols denote specimen numbers from each tow: -, 0; +, 1-4; ++, 5-9; +++ , Z10. n

IK, IKMT; ORI, ORI net. See text for detail. Estimates based on wire lengths/angles are underlined.

nn

H. Matsuura et al. / Deep-Sea Research II 57 (2010) 2098–2109

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Fig. 2. Vertical profiles of water temperature, salinity and dissolved oxygen at stations in the Celebes (A) and Sulu Seas (B).

Fig. 3. Vertical abundance distribution of augaptilid copepods (immature copepodids and adults) in the Celebes and Sulu Seas.

3.2. Vertical distribution of family and genera The vertical abundance patterns of Augaptilidae, the family as a whole, in the Celebes and Sulu Seas (Fig. 3) showed an essential absence of the copepods in the upper 75 m, peak abundances between 75-200 m, and a decrease in numbers with depth below 200 m both day and night, indicating the absence of a marked diel vertical migration. The peak abundances in the Celebes Sea (ca. 600 inds/1000 m3) were much lower than those in the Sulu Sea (ca. 6000 inds/1000 m3) by a factor of 10, and the decrease in numbers below 200 m was gradual and steady down to 1000 m in

the Celebes Sea, while in the Sulu Sea there was an abrupt decline in abundance below 200 m and an increase between 800-1000 m. Accordingly, the integrated water-column abundance of Augaptilidae in the upper 1000 m was higher in the Sulu Sea (day-night average: 418 inds m  2) than in the Celebes Sea (177 inds m  2) by a factor of 2.4 (Fig. 4A), while in the 200-1000 m layer it was similar between the Sulu and Celebes Seas at 121 inds m  2 (Fig. 4B). These patterns directly reflected the abundances and distribution of the genus Haloptilus, which contributed 50% (Celebes Sea) and 85% (Sulu Sea) to the integrated water-column abundance of

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Fig. 4. Integrated water-column abundance of augaptilid genera (immature copepodids and adults) in the Celebes and Sulu Seas. (A), 0-1000 m; (B), 200-1000 m.

Fig. 5. Vertical abundance distribution of augaptilid genera (immature copepodids and adults) in the Celebes and Sulu Seas.

Augaptilidae (Fig. 4A). The next-most abundant genus was Euaugaptilus, contributing 40% (Celebes Sea) and 10% (Sulu Sea) to the total abundance. While the genus showed a marked abundance peak in the 300-500 m layer (250-300 inds/1000 m3) during day and night in the Celebes Sea, the vertical distribution

was more even in the Sulu Sea with lower abundances at their peak ( o130 inds/1000 m3). Augaptilus, Centraugaptilus, Pseudaugaptilus, and Pseudhaloptilus occurred in much lower abundances ( o50 inds/1000 m3), with Pseudhaloptilus occurring only in the Celebes Sea (Fig. 5).

H. Matsuura et al. / Deep-Sea Research II 57 (2010) 2098–2109

3.3. Species diversity of Euaugaptilus A total of 29 species of the genus Euaugaptilus occurred in the 0-1000 m MOCNESS samples from the Celebes Sea, but only 8 species occurred in the Sulu Sea. All of these occurred also in the Celebes Sea, so the Sulu Sea contained no endemic or undescribed species (Table 3). In the Celebes Sea the number of species showed similar vertical patterns between day and night, increasing with depth to 10 species at 300-400 m, with a depression between 400-500 m, and reaching the maximum of 13 species in the 500-600 m layer (Fig. 6). In the Sulu Sea only 1 species occurred between 100-175 m and 3 to 6 species from 200-1000 m. The Shannon-Wiener index (H’) also increased with depth in both the Celebes and Sulu Seas, but with a marked minimum at 400-500 m in the Celebes Sea and at 500-800 m in the Sulu Sea, which are attributable to the predominance of a single species, E. palumbii in these layers (see next section). Species that occurred only in the samples from the ORI net and the IKMT that reached depths below 1000 m are indicated in Table 3. Among the 6 species from the Celebes Sea, only E. hyperboreus occurred also in the Sulu Sea. The other 7 species captured in the Sulu Sea occurred in the 0-1000 m MOCNESS samples from the Celebes Sea, suggesting that the 7 species inhabiting the mesopelagic layer in the Celebes Sea were distributed in deeper layers in the Sulu Sea.

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( o5 inds/1000 m3) between 200-1000 m in the Celebes Sea, but were mostly concentrated with much higher abundances ( 420 inds/1000 m3) at 800-1000 m in the Sulu Sea. Fig. 8 summarizes the vertical patterns of all the species collected with the MOCNESS in the Celebes Sea. The day/night data are pooled on the basis of the essential absence of diel vertical migration in the genus as shown in the present (Fig. 7) and previous studies (e.g. Roe, 1972; Weikert, 1982), and the

3.4. Vertical distribution and community structure of Euaugaptilus species Among the 8 species that occurred in the upper 1000 m of the Sulu Sea, the vertical patterns of the 6 most-abundant species are shown in Fig. 7, together with those of each species in the Celebes Sea. These species showed no marked diel vertical migration. However, there was a trend of shift or extension of the depth range into deeper layers in the Sulu Sea relative to the Celebes Sea, except for E. filigerus, which showed the reverse pattern. In particular, E. palumbii, which dominated in both the Celebes and Sulu Seas, was restricted mostly to the 300-600 m layer in the Celebes Sea but extended its population down to 1000 m in the Sulu Sea with more even abundances between layers. Euaugaptilus nodifrons showed an irregular pattern between 200-1000 m in the Celebes Sea, while it showed marked bimodal peaks at 200-300 m and 900-1000 m in the Sulu Sea. Euaugaptilus angustus and E. bullifer occurred in low and even abundances

Fig. 6. Vertical distribution of species numbers and diversity index (H0 ) in Euaugaptilus in the Celebes and Sulu Seas.

Table 3 Grouping of Euaugaptilus species according to their occurrence depths in the Celebes and Sulu Seas. ‘‘No occurrence’’ indicates that the species was present in the Celebes Sea but not in the Sulu Sea. Celebes Sea Sulu Sea

0-1000 m

Species

E. E. E. E. E. E. E. E.

No. of species

8

angustus bullifer filigerus gibbus hecticus longiseta nodifrons palumbii

0-1000 m 41000 m E. E. E. E. E. E. E.

7

laticeps latifrons longimanus magnus oblongus perodiosus rigidus

No occurrence E. E. E. E. E. E. E. E. E. E. E. E. E. E.

atlanticus digitatus elongatus facilis gracilis grandicornis marginatus maxillaris niveus penicillatus propinquus rectus roei tenuispinus

14

41000 m 41000 m

No occurrence

E. hyperboreus

E. E. E. E. E.

1

5

austrinus clavatus fecundus indicus matsuei

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Fig. 7. Vertical distribution of the six-most abundant species of Euaugaptilus in the Sulu Sea, compared with those in the Celebes Sea.

species are arranged in the order of estimated mean population depths. The water-column integrated abundance and the depth ranges representing 50% and 80% of each population are also shown, but only the layers of occurrence are indicated in the species that occurred in low numbers ( o0.5 inds m  2). It is noted that each species showed a limited vertical range within the mesopelagic depths (200-1000 m), occupying particular ranges from the upper-mesopelagic (e.g. E. filigerus and E. hecticus) to lower-mesopelagic zones (e.g. E. magnus and E. niveus). In addition, all 8 species that occurred in the upper 1000 m of the Sulu Sea (indicated in bold letters) had the major part of their population in the upper 400 m in the Celebes Sea, while the species that occurred only below 400 m in the Celebes Sea were mostly absent from the Sulu Sea, except for the 3 species that were collected below 1000 m in the Sulu Sea (indicated in brackets). The analysis of community structure based on the Bray-Curtis similarity index of species composition between samples from different stations (Stn 23, Celebes Sea; Stn 26, Sulu Sea), times (D, day; N, night), and depth ranges (Fig. 9) showed 4 distinct clusters at the level of 30% similarity, each comprised of the samples from (1) 100-400 m in both seas, (2) 150-175 m in both

seas, (3) 400-1000 m only for the Celebes Sea, and (4) 300-1000 m only for the Sulu Sea (4-1) and the shallowest layers (50-100 m) of the Celebes Sea (4-2) (note that 50-100 m Sulu samples were excluded from the analysis due to non-occurrence of Euaugaptilus spp.). Of these, cluster 2 and sub-cluster 4-2 represent extremely species-poor samples from the epipelagic depths ( o175 m), which appear to have resulted in their positions in the analysis deviating from those expected from their respective depth layers. The gross pattern indicates that the community structures of Euaugaptilus in the mid- to lower mesopelagic zone (400-1000 m) of the Celebes and Sulu Seas are totally different, while those in the upper mesopelagic zone ( o400 m) are much more similar between the two seas. In most of these clusters, the day/night samples from the same depths are of high similarity to each other, indicating negligible diel vertical change in species compositions.

3.5. Morphology of mouthpart appendages and body sizes There is a marked variety in the mouth appendage structures amongst the Euaugaptilus species, particularly in the ‘button setae’ on the maxillae and maxillipeds (Matsuura and Nishida, 2000)

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Fig. 8. Vertical distribution of all Euaugaptilus species in the Celebes Sea. Species in bold letters indicate species that also occurred in MOCNESS samples (0-1000 m) from the Sulu Sea. Species in brackets indicate species that were absent from MOCNESS samples but occurred in ORI net/IKMT samples that reached below 1000 m in the Sulu Sea. The water-column integrated abundances and the depth ranges representing 50% and 80% of the population are shown for species with abundances of 0.5 inds m  2 or more, but only the layers of occurrence are indicated for species of lesser abundance.

Fig. 9. Community structure of Euaugaptilus. Dendrogram derived from cluster analysis using log10-transformed abundance of species and the Bray-Curtis similarity index. Clustering based on group average linkage was applied to the between-sample similarity matrix. Stations were classified into 4 groups with 2 sub-groups (parentheses) at the 30% linkage level (dotted line). Stations (23, Celebes; 26, Sulu), depths, and day/night (D/N) traits for each cluster are summarized under cluster numbers.

and in the gnathobase of the mandible (hereafter referred to as ‘mandible blade’; see also Tanaka and Omori, 1974). In the 6 most-abundant species that co-occurred in the Sulu Sea there were 4 distinct types of these setae specific to the species or species groups, hereafter referred to as Types-A to D (Table 4). Type-A setae have a pair of parallel rows of semicircular buttons with the distal margin nearly straight and modified into a thin membrane; the buttons are modified into serrated processes near

the base of the setae (Fig. 10a, c: E. hecticus and E. palumbii). TypeB setae are similar to Type-A in the arrangement of buttons but the buttons are larger relative to the setal diameter (Fig. 10e: E. bullifer). Type-C setae have closely spaced buttons that are very small relative to the setal diameter; the buttons are long and elliptical proximally but truncate distally (Fig. 10g, i: E. angustus and E. filigerus). Type-D setae are markedly different from the other types and have a pair of parallel rows of well-developed

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Table 4 Comparison of vertical ranges, body sizes, and types of feeding appendages of the 6 species that occurred in the upper 1000 m in the Sulu Sea. Species of Euaugaptilus

Setal type

Mandible type

female prosome length [mm: mean 7 SD (n)]

Main vertical range (m)

E. E. E. E. E. E.

A A B C C D

I II II I I III

1.86 7 0.15 1.66 7 0.03 3.20 (2) 4.10 (2) 4.29 7 0.12 4.54 7 0.58

100-600 400-600 900-1000 200-400 900-1000 200-300, 900-1000

hecticus palumbii bullifer filigerus angustus nodifrons

(16) (129)

(29) (14)

Fig. 10. SEM images of button setae (a, c, e, g, i, k) and mandible blades (b, d, f, h, j, l ) of 6 species of Euaugaptilus that occurred in the Sulu Sea. a, b: E. palumbii. c, d: E. hecticus. e, f: E. bullifer. g, h: E. angustus. i, j: E. filigerus. k, l: E. nodifrons.

comb-like setules though the length of the endopod setae of the maxilliped, while the setae of the maxilla bear 4 rows of setules partly modified into thin plates (Fig. 10k: E. nodifrons). Regarding the mandible blade, 3 types were discernible in the Sulu-Sea species (Table 4; see also Grice and Hulsemann, 1965; Tanaka and Omori, 1974; Park, 1993). Type-I blade is like a curved needle and has 2 (Fig. 10d: E. hecticus) or 4 spiniform teeth (Fig. 10h, j: E. angustus and E. filigerus). Type-II blade is narrow, flattened and has 3 pairs of cuspidate or spiniform teeth (Fig. 10b, f: E. palumbii and E. bullifer). Type-III blade is broad and with 11 cuspidate teeth of varying size (Fig. 10l: E. nodifrons). The body sizes (PL of adult female) of the species that occurred in the Sulu Sea differed considerably, from the smallest E. palumbii (mean: 1.7 mm) to the largest E. nodifrons (4.5 mm) (Table 4).

4. Discussion 4.1. Distribution of family and genera The present observations are consistent with previous records in that the family Augaptilidae comprises genera that are predominantly meso- and bathypelagic with most species

performing little diel vertical migration except for the genus Haloptilus which, while being a non-migrant as well, often predominates in the shallower layers within the vertical range of the family and occurs in the epipelagic zone as well (e.g. Grice and Hulsemann, 1965; Deevey and Brooks, 1977; BradfordGrieve, 1999). The dominance of Haloptilus in the epipelagic zone with its apparent avoidance of the surface mixed layer of high temperature water has been reported in semi-enclosed basins such as the Mediterranean (Scotto di Carlo et al., 1984; Weikert and Trinkaus, 1990) and the Red Sea (Weikert, 1982), and this was also the case in the Celebes and Sulu Seas. While there is no mention of the physical parameters in the paper by Scotto di Carlo et al. (1984) on the Tyrrhenian Sea, in the eastern Mediterranean there was only a slight decrease in temperature (from 16.5 to 14.0 1C) and salinity (from 38.9 to 38.8) in the layers dominated by Haloptilus species (Weikert and Trinkaus, 1990). In the central Red Sea, however, the 100-250 m layer which was dominated by H. longicornis coincided with the layer of the oxycline (from 4.5 to o1.5 mlO2l  1) and a sharp gradient of temperature (from 27.7 to 21.7 1C) and salinity (from 40.0 to 40.5), which was apparently avoided by other calanoids and pteropods (Weikert, 1982). An association of Haloptilus chierchiae with the lower oxycline of the oxygen-minimum zone in the Arabian Sea has also been reported

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by Wishner et al. (2008). The major distributional ranges of epipelagic Haloptilus in the Celebes and Sulu Seas (75-200 m) coincide with steep gradients in temperature, salinity and oxygen content (Fig. 2). Interestingly, marked depressions in the total copepod biomass (wet weight) have been observed in the 75-100 m layer in the daytime both in the Celebes and Sulu Seas (Nishikawa et al., 2007). This appears to be consistent with the observation by Weikert (1982) in the Red Sea, suggesting that Haloptilus species can exploit the subsurface layers of tropical waters with steep environmental gradients, such as in temperature, salinity, and oxygen content, more effectively than other copepods (see also Saltzman and Wishner, 1997). The other genera showed trends of either more even distribution extending to deeper layers (Euaugaptilus and Augaptilus), more concentrated distribution in particular depths (Pseudaugaptilus and Centraugaptilus), or total absence (Pseudhaloptilus) in the Sulu Sea relative to the Celebes Sea, suggesting differential responses of each taxonomic group to different water-column structure. Comparison with other sea areas, however, is presently impossible, due to a lack of information on the vertical patterns of these extremely-rare copepods. 4.2. Patterns of abundance and species diversity in Euaugaptilus The vertical patterns of abundance and number of species in Euaugaptilus in the Celebes Sea appear to follow the pattern that has been commonly observed in various groups of oceanic zooplankton (e.g. Grice and Hulsemann, 1965; Vinogradov, 1968; Roe, 1972; Deevey and Brooks, 1977; Kuriyama and Nishida, 2006) in that peaks in abundance are located shallower than the peaks in species number and the latter increases with depth to reach its maximum in the lower mesopelagic zone. This indicates that the upper mesopelagic zone is characterized by a small number of abundant species while the lower mesopelagic zone has a larger number of species but at lower abundances. In the Celebes Sea there was a reduction of both the species number and the Shannon-Wiener index (H0 ) in the mid-layer (400-600 m: Fig. 6), which can be ascribed to the high abundance of E. palumbii and the associated exclusion of several non-dominant species in that layer. In contrast, the much lower number of species throughout the mesopelagic zone of the Sulu Sea indicates that the reduction of the total species number is mainly due to the absence of many species in the middle- and lower mesopelagic zones. 4.3. Species richness and community structure in Euaugaptilus A total of 29 species of Euaugaptilus were collected from the present MOCNESS samples from the upper 1000 m of the Celebes Sea and the collection that covered layers below 1000 m added 6 more species, resulting in a total of 35 species (Table 3). This number represents 48% of the species currently known (73 species: Boxshall and Halsey, 2004) and is higher than previous records of comparable, or even more extensive, coverage in sampling depths and total filtered volume : 13 species from the NE Atlantic (0-5000 m: Grice and Hulsemann, 1965), 25 species from the NE Atlantic (40-960 m: Roe, 1972), 31 species from the Izu Region, Japan (0-2500 m; Tanaka and Omori, 1974), 19 species from the Sargasso Sea (0-2000 m: Deevey and Brooks, 1977), 14 species from the Antarctic and Subantarctic waters (0-3660 m: Park, 1993) and 13 species from the Southwest Pacific (0-1697 m: Bradford-Grieve, 1999). In contrast, only 8 species were recorded from the 0-1000 m series in the Sulu Sea with 8 species being added from the deeper tows, resulting in a total of 16 species which, however, is still

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much larger than the species numbers reported from semienclosed seas with similar hydrographic conditions such as the eastern Mediterranean (2 species, E. hecticus and E. filigerus: Scotto di Carlo et al., 1984) and the Red Sea (1 species, E. hecticus: Weikert, 1982); both of these species occurred in the Sulu Sea. It should be noted that the species of the genus Euaugaptilus are among the most sparsely distributed copepods in the oceans, hence the possibility of underestimating the number of species occurring in the study area cannot totally be ruled out. However, in addition to the MOCNESS sampling, the repeated sampling in the Sulu Sea (9 times) with the ORI net and the IKMT makes it possible to conclude true absence of a considerable number of species in the Sulu Sea, at least for the 0-1000 m water column. These differences in species richness between the two seas are clearly reflected in the community structure (Fig. 9), which showed marked differences between the mid- to lower mesopelagic zones of the Celebes and Sulu Seas in contrast to the higher similarities in the upper mesopelagic. The major depth boundary of these clusters appears to exist at ca. 400 m, suggesting that the deepest sill depth (420 m) in the Mindoro Strait, enabling mixing of the epipelagic and upper mesopelagic waters of the Sulu Sea with the surrounding waters, is one of the key factors for the observed differences in the community structure between the seas.

4.4. Factors determining species richness The present observation demonstrated an extremely high species richness of Euaugaptilus in the Celebes Sea and its considerable reduction in the Sulu Sea, which appears to coincide with the presence of the homogenous, warm water in the mesoand bathypelagic zone of the Sulu Sea. Interestingly, out of the 8 species that occurred in the 0-1000 m layer of the Sulu Sea, 4 species were the top-four dominants in the Celebes Sea and the upper limit of their vertical range extended to the upper 400 m, while most of the other species that occurred only in the Celebes Sea occurred at low abundances ( o0.5 inds m  2) and had their center of distribution in the mesopelagic layers deeper than 400 m where the temperature was 4-6 1C lower than in the midwater in the Sulu Sea. On the other hand, among the 8 species from the Sulu Sea that were collected only by the deep ( 41000 m) tows, 6 species (E. latifrons, E. magnus, E. oblongus, E. rigidus, E. perodiosus, and E. hyperboreus) were collected only below 400 m in the Celebes Sea. In particular, E. perodiosus and E. hyperboreus, which were collected in the Celebes Sea only from 900-1000 m and below 1000 m, respectively, appear to have successfully established their population in the bathypelagic zone of the Sulu Sea, despite the temperature difference of 6 1C or more. This indicates that the elevated mid-water temperature is not the only factor responsible for the observed reduction in species richness in the Sulu Sea; while many species in the mid-water of the Celebes Sea appear to be unable to tolerate the 10 1C deep-water of the Sulu Sea, there are still some species that can tolerate this high-temperature environment. Other factors that may be related to the observed reduction in species richness in the Sulu Sea include (1) possible exclusion of species through competition in the extremely homogenous environment in the Sulu Sea, in contrast to the coexistence of many species through resource partitioning along an environmental gradient that is moderate and stable in the mesopelagic zone of the Celebes Sea, (2) reduced dissolved-oxygen content in the Sulu Sea relative to the Celebes Sea, which might adversely affect survival of some species, and (3) possible reduction in the diversity of predators in the Sulu Sea. Of these, the influence of dissolved-oxygen content may not be so crucial, considering the

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low oxygen consumption rates of augaptilids (Thuesen et al., 1998) and the oxygen levels of 41.5 ml l  1 in the upper 1000 m of the Sulu Sea, which is above the critical concentration necessary for most deep-sea copepods (e.g. Longhurst, 1985; Thuesen et al., 1998; Wishner et al., 2000). Predation impact may also be of minor significance, because of the fairly low abundance of Euaugaptilus copepods within the copepod communities in meso- and bathypelagic waters; previous gut-content analyses of mesopelagic fishes, which are assumed to be among their major predators, have indicated non-occurrence of Euaugaptilus copepods (Hopkins and Sutton, 1998). However, there are many other potential predators that should be considered, which would make a quantitative analysis practically impossible (Longhurst, 1985). Coexistence of a large number of species in an environment with predictable, stable physico-chemical gradients has been suggested for the copepod assemblages at the BIOSTAT station in the eastern tropical Pacific, in which the highest species richness is maintained in the zone of a steep pycnocline (Longhurst, 1985), and this also appears to be the case in the mesopelagic water of the Celebes Sea, which accommodates 35 species or more of Euaugaptilus in a quasi-steady, moderate gradient of temperature. Disappearance of this gradient in the Sulu Sea, with the mesopelagic water being extremely homogenous, may have resulted in the exclusion of more than 2/3 of the species through competition with ‘more-favored’ species that extended their vertical range into deeper and/or wider zones than in the Celebes Sea. Reduction of species richness in zooplankton has been reported from semi-enclosed basins with homogenous deepwater of high temperature, such as those in the Mediterranean (12-14 1C: Vinogradov, 1968; Scotto di Carlo et al., 1984; Weikert and Trinkaus, 1990) and the Red Sea (22 1C: Weikert, 1982), in which common bathypelagic species are absent or reduced in abundance and the deep waters are inhabited essentially by a few mesopelagic species typical of oceanic waters. It has been hypothesized that the Mediterranean basin was disconnected from the Atlantic Ocean during the last glacial period and most of the animals became extinct (Wright, 1979). Re-colonization by deep-sea species was hampered by the shallow sill at the Strait of Gibraltar. Reduced organic matter and high deep-water temperatures additionally caused the reduction of species richness in the bathypelagic zone of the eastern Mediterranean (Weikert and Koppelmann, 1993). The present situation in the Sulu Sea appears more-or-less similar to that in these seas, with their hightemperature and homogenous deep waters, but the number of Euaugaptilus species per se is much higher in the Sulu Sea. This may be attributable to the lower temperature (ca. 10 1C) of the meso- and bathypelagic waters in the Sulu Sea than in the Mediterranean and Red Sea and also to the high species richness in the surrounding waters (i.e. tropical western Pacific, including the Celebes Sea) which is among the most species-rich regions of the world oceans and might have been the source of the Sulu Sea fauna. On the basis of biostratigraphic and sedimentary analyses, it is suggested that the Sulu Sea originated as a back-arc or intraarc basin in the early to middle Miocene, and the isolation of the basin from deep waters of the Pacific occurred 1.9 million years ago (Anonymous, 1989). Recent discoveries of new hyperbenthic copepods from deep waters (1260-2450 m) of the Sulu Sea (Ohtsuka et al., 2005) suggests that its deep-water fauna was part of the greater western Pacific fauna before the establishment of the sills, and many deep-water species that were enclosed within the basin were unable to maintain their populations against historical changes of the physical properties of the deep water from typical oceanic conditions to the present hightemperature, low-oxygen and homogenous condition. Other species were able to successfully maintain their populations, or

evolved into species distinct from their open-water relatives, as is the case with at least some hyperbenthic copepods (Ohtsuka et al., 2005). This presumed difference in the geologic history between the Sulu Sea and the Mediterranean may partly explain the much higher species richness of Euaugaptilus in the former than in the latter. In addition, there were no marked differences in the slope of the decline with depth of the zooplankton biomass in the mesopelagic zone between the Sulu and the adjacent Celebes and South China Seas (Nishikawa et al., 2007), suggesting similar levels of organic flux into the mesopelagic zone in all of these seas. This is consistent with the observation that the standing stock of the Augaptilidae as a whole in the 200-1000 m layer is similar between the Sulu and Celebes Seas, suggesting that the few species that have successfully established their populations in the Sulu Sea are effectively exploiting the vacant niches of the excluded species.

4.5. Niche partitioning among co-occurring congeners in the Sulu Sea In contrast to the high species richness in the Celebes Sea, which is a case of coexistence of an extremely large number of congeneric species, the much reduced species diversity of Euaugaptilus in the Sulu Sea, along with its highly stable and homogenous mid-water environment, provides a setting with a simplified species assemblage that would enable us to examine possible mechanisms for the species’ co-existence. In addition, there is physiological and morphological evidence suggesting that Euaugaptilus copepods are ambush predators (Thuesen et al., 1998) that prey on small crustaceans such as copepods by using their button setae (Boxshall, 1985; Matsuura and Nishida, 2000). Hence information on body sizes and mouthpart structures will provide a measure of the food sizes and/or feeding tactics of these copepods. While the exact functional differences between these types of appendages are not known, it is expected that they are closely related to the physical and/or behavioral properties of potential prey, since the setal armature will be in direct contact with the food particle and each armature type will have an affinity with a specific surface structure and/or movement type of prey (Boxshall, 1985; Matsuura and Nishida, 2000), and this will also be reflected in the structure of the mandible blades (Itoh, 1970). Table 4 summarizes the vertical ranges, body sizes, and types of feeding appendages of the 6 species that occurred in the upper 1000 m in the Sulu Sea, excluding E. longiseta and E. gibbus whose depth ranges are uncertain due to their low abundances. There are 3 groups of species occurring in largely different depth layers. E. hecticus and E. filigerus occupy the upper-mesopelagic zone (200-400 m) with a considerable overlap, but the former is much smaller than the latter ( o1/2 in PL) and their mouthpart setae are of quite different types (Type A vs C), suggesting their niche partitioning is due to differentiation in their feeding tactics. E. palumbii and E. nodifrons are distributed widely from 200 to 1000 m with a considerable overlap, but the former was centered around 400-600 m while the latter showed a bimodal distribution with peaks at 200-300 m and 900-1000 m, showing complementary vertical distribution patterns. They also showed differences in body size (by a factor of 3) and in the morphology of the button setae (Type A vs D) and the mandible blade (Type II vs III). In particular, the latter two characters, i.e. the comb-like setules on the setae of maxilla and maxillipeds and the broad mandible blade with many (11) cuspidate teeth, in E. nodifrons appear to suggest suspension feeding as compared with those of E. palumbii which suggest carnivory. E. bullifer and E. angustus occupied the deepest layer (900-1000 m) and showed differences in PL (by a factor of 1.5) and in mouth appendage morphology (Type B vs C).

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These comparisons suggest that the species co-occurring in the homogenous mesopelagic zone of the Sulu Sea are differentiating their niches either with respect to their habitat depths, prey sizes, feeding tactics, or through combinations of these factors, except for the 2 species whose vertical ranges are unknown. It is also suggested that physical factors that are almost homogenous in the mesopelagic zone of the Sulu Sea, such as temperature, salinity, and dissolved-oxygen content, play only a minor role in determining the vertical range of each species. This suggests the potential importance of depth-related variables, such as pressure, light intensity, and quality and quantity of prey-resources, or the importance of biological interaction between the copepod species themselves, but this is still an open question. The situation in the Celebes Sea is much more complex than in the Sulu Sea due to the much larger number of co-occurring species, including non-dominant or extremely-rare species, a situation that makes an analysis of niche partitioning essentially impossible, inviting further research into their distributional patterns, coupled with feeding ecology and physiology. This, coupled with the present results, will lead to a better understanding of the functional aspects and provide data to enable future prediction of the response of highly diverse mesopelagic communities in the open ocean to environmental changes associated with global warming.

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