Data Al

Phycologia (****) Volume ** (*), *** *** Published 1 March 2007

Temporal and spatial comparison of the relative abundance of macroalgae

across the Mariana Archipelago between 2003 and 2005

ALINE D. TRIBOLLET PETER S. VROOM*

AND

Joint Institute for Marine and Atmospheric Research, University of Hawaii, NOAA Fisheries Service, Paci c Islands Fisheries

Science Center, Coral Reef Ecosystem Division, 1125 B Ala Moana Boulevard, HI 96814, USA

A.D. TRIBOLLET AND P.S. VROOM. 2007. Temporal and spatial comparison of the relative abundance of macroalgae across

the Mariana Archipelago between 2003 and 2005. Phycologia 46: 187 197. DOI: 10.2216/06-46.1

Past studies have argued that macroalgae serve as useful bioindicators that herald possible environmental changes to reef

ecosystems because they are often opportunistic, having high growth rates and responding quickly to environmental changes,

such as increased nutrient availability, grazing pressures, or storm activity. In this study, we test their usefulness as reef

monitoring management indicators. We investigated the spatial and temporal variability of the relative abundance of ma-

croalgae (RAM) at the genus level in the Mariana Archipelago between two surveys in 2003 and 2005. Islands vary

drastically across the archipelago (carbonate vs volcanic, populated vs unpopulated, small vs large) and often experience

considerable storm activity. We showed that the diversity of macroalgal genera was generally highest at the southern end

of the archipelago, probably because of increased habitat heterogeneity around these geographically larger islands. At the

northern end of the archipelago, only Pagan and Maug were large enough or contained enough environmental diversity to

exhibit macroalgal diversity similar to that of the southern carbonate islands. Despite the ubiquitous nature of turf algae,

crustose coralline red algae, and the green alga Halimeda (Bryopsidales) across the archipelago, multivariate analyses

revealed RAM to differ among islands with northern, unpopulated, volcanic islands grouping together and differing from

southern, populated, carbonate islands. Also, RAM showed signi cant variability at the local scale (among sites within an

island) and over time. We hypothesize that this variability results principally from differing oceanographic conditions such

as sea surface temperature, human impacts such as shing and pollution, typhoons, and volcanic activity across the archi-

pelago. These results provide a baseline for future monitoring studies in the Mariana Archipelago and suggest that rapid

ecological assessments of macroalgae in the eld at the genus level are a reliable indicator that can be used to monitor

change over time.

KEY WORDS: Algae, Coral reef, Mariana Archipelago, Northwestern Hawaiian Islands, Relative abundance, Spatial vari-

ability, Temporal change

INTRODUCTION glimpse of the constitution of algal communities in healthy

tropical reef environments and (2) serve as a direct point of

In tropical reef ecosystems, algal functional groups including comparison with reefs around heavily populated islands lo-

crustose coralline red algae, turf algae, and eshy macroalgae cated at the southern end of the archipelago. Although our

are abundant and widely distributed, contributing to the reef phycological knowledge of Guam is well established (Merten

framework, sedimentation, and the food chain (Adey 1998; 1971; Tsuda 1972a, b, 1974, 1977, 2003; Tsuda & Kami 1973;

Chisholm 2003). Both healthy (Vroom et al. 2005a) and de- Gordon et al. 1976; Paul & Van Alstyne 1988, 1992; Lobban

graded (Lapointe et al. 2004; Fabricius et al. 2005) reefs et al. 2002), the remote location and challenging working con-

where macroalgal communities dominate serve as sinks for ditions around many of the northern Mariana Islands have

atmospheric CO2 because of high rates of net primary pro- greatly limited phycological studies. Only two lists of ma-

duction (Kayanne et al. 1995; Gattuso et al. 1996a, b, 1997; croalgal species that include all 15 islands in the archipelago

Kraines et al. 1996). Because algal functional groups are often are available (Tsuda & Tobias 1977a, b; Tsuda 2003). These

opportunistic (Adey 1998), having high growth rates and re- studies report a total of 332 species of benthic marine ma-

sponding quickly to environmental changes (Thacker et al. croalgae, with most species known only from Guam and Sai-

2001; Hallock 2005) such as increased nutrient availability

pan (Tsuda 2003). The number of species collected from the

(Hunter & Evans 1995; Fabricius et al. 2005; Lapointe et al.

unpopulated islands of the archipelago ranges from 1 (for Sar-

2005a, b), grazing pressures (Adey 1998; Szmant 2002), or

igan) to 52 (for Maug) and will increase substantially as ad-

storm activity (Vroom et al. 2005b), they may serve as useful

ditional marine algae collected during our expeditions are tax-

bioindicators that herald possible environmental changes to

onomically identi ed (R. Tsuda, personal communication).

coastal ecosystems (Le Bris et al. 1998; O Shanahan et al.

In October 2003 and October 2005, as part of the NOAA

2003; Barile 2004).

Coral Reef Conservation Program s Mariana Archipelago

To better understand and conserve tropical reefs as a whole,

Reef Assessment and Monitoring Program (MARAMP), the

remote ecosystems with little anthropogenic activity can serve

Coral Reef Ecosystem Division (CRED), Paci c Islands Fish-

as models for comparison with disturbed reef environments.

eries Science Center of the NOAA Fisheries Service, con-

In remote areas such as the northern Mariana Islands, algal

ducted algal surveys at all islands and several submerged

functional groups have been poorly studied. Examining algal

banks in the Mariana Archipelago. These efforts are the rst

populations in these areas can (1) provide researchers with a

to provide quantitative algal data for the entire archipelago

and investigate the variability of the relative abundance of

* Corresponding author (abp2dj@r.postjobfree.com).

187

188 Phycologia, Vol. 46 (2), 2007

macroalgae (RAM) at the genus level at 15 islands and banks

over a two-year period (2003 2005). Our objectives were to

(1) determine RAM at each island in the Mariana Archipelago

for both 2003 and 2005, (2) deduce if RAM differed spatially

among sites/islands within each sampling period, and (3) ex-

amine if RAM changed among sites/islands over time.

MATERIAL AND METHODS

Location

Wedged between the Philippine Sea to the west and the Paci c

Ocean to the east, the Mariana Archipelago contains 15 major

islands and numerous banks and shoals that stretch for 750

km along a north-to-south axis (Fig. 1). Fourteen islands be-

long to the US Commonwealth of the Northern Mariana Is-

lands (CNMI), while the southernmost island belongs to the

US Territory of Guam.

Guam, Rota, Tinian, and Saipan represent the largest, south-

ernmost inhabited islands in the archipelago. Although they

have a volcanic origin, each island is now capped by a raised

carbonate platform protected by barrier and well-developed

fringing reefs to the west (leeward side) (Gilman 1997; Rich-

mond et al. 2002). Guam, the largest of these islands (560

km2) contains numerous reef habitats (fringing reefs, barrier

reefs, reef slopes, and lagoon and patch reefs). Guam also

shows high biodiversity with 306 species of macroalgae and

403 species of hard corals reported (Richmond et al. 2002).

The southern carbonate islands, except Aguijan, which is un-

inhabited, experience varying levels of anthropogenic stress

including shing, sewage, pollution, dredging, and sedimen-

tation that reduce water quality and smother nearshore corals

(Richmond et al. 2002; Abraham et al. 2004; Bearden et al.

2005). Santa Rosa is a submerged carbonate bank located

southwest of Guam and is reported to experience some shing

pressure (Abraham et al. 2004; personal observation).

The northern nine islands (Uracas, Maug, Asuncion, Agrihan,

Pagan, Alamagan, Guguan, Sarigan, and Anatahan) are distinct

from their southern counterparts and represent small, uninhabit-

ed, active strato-volcanoes that rise steeply from the ocean oor.

Although most of these northern islands are volcanic cones,

Maug consists of three small islands surrounding a ooded cal-

dera. The coral reefs around most of the northern islands exhibit

limited coral development, and some have experienced sedimen-

tation due to deforestation by feral animals and volcanic activity

(Richmond et al. 2002). The ash fallout from the 2003 and 2005

eruptions at Anatahan Island caused extensive damage to near-

shore reef habitats (Bearden et al. 2005).

In general, limited in situ oceanographic data are available

Fig. 1. Map of the Mariana Archipelago.

for the Mariana Archipelago. Sea surface temperature (SST)

varies seasonally (Fig. 2), ranging between 24.5 C and

30.5 C at the northern end of the archipelago (Maug), with a four typhoons and four tropical storms (Table 1) passed over

smaller range of 25.5 C to 30.0 C at the southern end of the the archipelago, affecting primarily the southern islands. The

archipelago (Guam). Between October and November, the last typhoon occurred in August 2005 at the beginning of our

northern islands typically experience temperatures at least 1 C research expedition, affecting primarily the islands of Saipan

cooler than their southern counterparts. October 2005 salinity and Tinian.

measurements varied between 34.2 and 34.7 from south to Very few prior data concerning reef health are known for

north (R. Hoeke, personal communication). In regard to most of the archipelago. A major crown-of-thorns star sh

weather, the Mariana Archipelago experiences frequent ty- (COTS) outbreak was reported in 1978 around Rota, Saipan,

phoons and tropical storms, especially from August to No- and Tinian (Quinn & Kojis 2003), but since that event, the

vember. For example, between June 2002 and October 2003, density of COTS has remained low around those islands

Tribollet & Vroom: Macroalgae of the Mariana Islands 189

Fig. 2. Path nder satellite Sea Surface Temperatures (SST) from Maug, Pagan, Saipan, and Guam: January 1985 January 2005. Red line

indicates temperature at which coral bleaching is known to occur. (Figure made by Ronald Hoeke.)

Table 1. Typhoon activity in Guam and CMNI: June 2002 August 2005. Storm statistics from http://weather.unisys.com/hurricane/w_paci c/.

Wind speed (km h 1)

Storm Date Latitude Longitude Islands closest to storm path

Typhoon #8 Jun. 2002 13.3 145.7 167 Guam

13.8 144.2 176 Guam

14.2 143.2 200 Rota

Typhoon #10 Jul. 2002 12 144.2 176 Santa Rosa, Guam

Typhoon #25 Oct. 2002 18 145.8 120 Pagan, Alamagan

18.6 144 139 Pagan, Agrihan

Typhoon #31 Dec. 2002 12 146.2 204 Guam

14.3 144.7 240 Rota

15.2 144.2 231 Saipan, Anatahan

Typhoon Tinting Jul. 2004 16.2 146.4 120 Anatahan

16.8 145.7 139 Sarigan

17.6 144.9 139 Pagan, Alamagan

Supertyphoon Chaba Aug. 2004 14.4 146.3 203 Rota

14.4 145.4 231 Rota

17.6 144.9 139 Aguijan

Supertyphoon Songda Aug./Sep. 2004 17.8 146.7 241 Pagan, Alamagan

18.4 146.3 231 Pagan, Agrihan

19.6 145.4 231 Asuncion

Typhoon Haitang Jul. 2005 21.3 145.9 130 Uracas

20.5 144.7 139 Uracas

Typhoon Nabi Aug. 2005 15.6 146.3 167 Saipan, Tinian

16.5 145.0 176 Anatahan

190 Phycologia, Vol. 46 (2), 2007

(Quinn & Kojis 2003) and more generally across the archi- Mariana Archipelago or within individual islands, several

pelago (Richmond et al. 2002). Coral bleaching has been not- two-way crossed ANOSIMs were conducted. In the rst anal-

ed in CNMI and Guam several times since 1994 (Richmond ysis, 46 sites from across the Mariana Archipelago sampled

et al. 2002), but no quantitative assessment exploring the spa- in both 2003 and 2005 were compared (Appendix 1; Factor

tial extent of these events was made (Bearden et al. 2005). A year, Factor B site; 5000 permutations). In the other

analyses, temporal changes were examined at each island in-

Survey technique dependently of other islands (Factor A year, Factor B

site; 5000 permutations).

As part of the MARAMP surveys, CRED quantitatively as-

sessed algal populations at 64 sites in 2003 and 70 sites in

2005 at 15 islands and three submerged banks in the Mariana

RESULTS

Archipelago (Appendix 1). At each island surveyed, long-term

monitoring sites were selected by a multidisciplinary group of

Diversity

researchers to represent a variety of habitat types that could

be accessed on a biennial basis regardless of prevailing weath-

Forty-seven genera of eshy macroalgae were found at sites

er or oceanographic conditions. At each site, phycologists

sampled across the Mariana Archipelago (35 genera in 2003,

used SCUBA to sample two 25-m transect lines set in a sin-

47 genera in 2005; Table 2). Additionally, six algal functional

gle- le row, with each transect separated by 10 m. A 0.18-

groups including cyanophytes, branched nongeniculate coral-

m2 sampling quadrat was located at randomly selected points

line red algae, crustose coralline red algae, brown algal crusts,

along each transect (three points per transect), and another

orange algal crusts, and turf algae (dominated by red algal

quadrat was located at a point 3-m perpendicular from each

species of the order Ceramiales) were documented. Southern

random point in the direction of shallower water; altogether,

carbonate islands generally exhibited a higher diversity of ma-

there were 12 quadrats per site. The usefulness, ef ciency, and

croalgal genera than northern volcanic islands, although there

accuracy of this protocol have has been demonstrated by Pres-

was no statistical difference between islands (Tables 2, 3). In

kitt et al. (2004), Vroom et al. (2005a, 2006), and Vroom &

2003 and 2005, turf algae, crustose coralline red algae, and

Page (2006). Fleshy macroalgae were identi ed to genus in

species of the green algal genus Halimeda Lamouroux were

the eld, whereas cyanophytes, branched nongeniculate cor-

the most common algae to occur in quadrats across the Mar-

alline red algae [e.g. Neogoniolithon brassica- orida (Har-

iana Archipelago (Table 2). Other ubiquitous although less

vey) Setchell & Mason; R. Tsuda, personal communication],

prevalent genera or functional groups included the chlorophy-

crustose coralline red algae, brown algal crusts, orange algal

te Neomeris Lamouroux, the phaeophyte Dictyota Lamou-

crusts, and turf algae were lumped into functional group cat-

roux, the rhodophyte Jania Lamouroux, and nongeniculate

egories, their identi cation being dif cult or impossible un-

branched coralline red algae. Lobophora Agardh, a genus of

derwater. Ranks were assigned to each genus or functional

brown algae, commonly occurred around northern islands dur-

group found in each quadrat (1 being the most abundant in

ing both sampling periods but was not observed around south-

terms of number, 2 being the next most abundant, etc., with

ern islands during 2003 and was rarely observed during 2005.

10 being the maximum number of genera found in a single

Several differences were observed in algal prevalence within

quadrat) to determine RAM.

sampled quadrats between 2003 and 2005. Dictyota and Jania,

two genera commonly seen in abundance across the archipelago

Statistical analysis

in 2005, were observed only sporadically in 2003. On a more

To test signi cant differences of RAM among sites and is- regional level, cyanophyte populations seemed to decrease in

lands, a matrix was created that included genus and functional abundance at northern islands between 2003 and 2005 (Table 2).

group ranks from quadrats surveyed in 2003 and 2005. Each Similarly, Dictyosphaeria Decaisne, Microdictyon Decaisne,

quadrat was treated as an individual replicate within a site for Galaxaura Lamouroux, and Padina Adanson were common in

each year (n 12 quadrats/site), and a Bray Curtis similarity southern islands during 2003, but by 2005 only Dictyosphaeria

matrix of untransformed rankings by quadrat was created us- remained a common component of areas sampled. Neomeris was

ing PRIMER 5.2.9. (Clarke & Warwick 2001). For each year the only genus whose relative abundance increased at southern

surveyed, a two-way nested analysis of similarity (ANOSIM; islands from 2003 to 2005. The chlorophyte Chlorodesmis Har-

5000 permutations) nesting sites within island (n 64 sites vey & Bailey was common at most islands during both research

for 2003, n 70 sites for 2005) was conducted to determine expeditions but was especially abundant in northern islands dur-

if differences in similarities occurred among sites and islands. ing the 2005 sampling period.

These analyses were followed by two similar ANOSIMs, one

for each year, using only common sites surveyed both in 2003 Spatial variability

and 2005 (n 46 common sites; 5000 permutations).

To depict relationships among islands (latitudes) based on The two-way nested ANOSIMs of ranked data from 64 and

RAM, data within the matrices were averaged by island for 70 sites in 2003 and 2005, respectively, showed that RAM

each year, and a Bray Curtis similarity matrix of the averaged did not vary across the archipelago as a whole (no difference

data was generated. Ordinations of relationships were created among islands, r values 0.25 and P 0.001; Table 3) but

via nonmetric multidimensional scaling (nMDS; 30 restarts) highlighted moderate differences of RAM among sites within

and these relationships visually compared to geographic maps islands (r values 0.4, P 0.001). The two-way nested AN-

of the archipelago. OSIMs using only sites common to both 2003 and 2005 sug-

To determine if RAM changed over time across the entire gest minimal differences of RAM among islands (r values

Tribollet & Vroom: Macroalgae of the Mariana Islands 191

Table 2. Percentage of quadrats at each island in which macroalgal genera were found in 2003 and 2005. Year 2003 data are represented by

numbers without parentheses; 2005 data are represented by numbers in parentheses. Symbols are used for genera that occurred in 20% of

quadrats; 2003 data, 2005 data. Crust. Coralline, crustose coralline red algae; branch. corall., nongeniculate branched coralline red

algae; Laurencia/Ch, Laurencia/Chondrophycus; SAN, Santa Rosa; GUA, Guam; ROT, Rota; AGU, Aguijan; TIN, Tinian; SAI, Saipan; SAR,

Sarigan; ALA, Alamagan; PAG, Pagan; AGR, Agrihan; ASU, Asuncion; MAU, Maug; URA, Uracas.

Genus/group SAN GUA ROT AGU TIN SAI SAR ALA PAG AGR ASU MAU URA

Island size (km2) Submerged 541-**-*-***-*** 5 11 48 30 7 2 3

Human population 0 168,564-****-*-**** 62,392 0 0 0 0 0 0 0

No. genera **-**-**-**-**-** **-**-**-**-**-** 9

No. functional groups 2 4 5 6 5 5 5 5 5 5 4 4 2

Functional groups

Branch. corall (**-**-**-**-**-** 55 64

Brown crusts

Crust. coralline 81 (64) 46 (47) 75 (86) 47 (46) 47 (73) (56) 67 (83) 42 (75) 53 (56) 22 (78) 43 (43) 25

Cyanophytes (58) 56 (52) 48 (89) 38 (61) (64) 22 (50) 44 43 (23) 28 50 22

Orange crust

Turf algae 100 (88) 98 (100) 100 (97) 96 (100) 89 (97) 100 (95) 94 (91) 100 (100) 94 (96) 86 (97) 97 (97) 83 (81) 100 (89)

Green algae

Anadyomene

Avrainvillea (63) 42

Boodlea 22 63

Bornetella 42

Bryopsis

Caulerpa (**-**-**-**-**-** 58

Chlorodesmis 79 25 (31) 25

Codium (21)

Dictyosphaeria 75 (79) 25 (32) 25 (39) 22

Halimeda 58 (92) 51 (95) 60 (67) 33 (31) 61 (60) 75 (58) 44 (30) 41 25 (28) 25 (32)

Microdictyon 100 (67) 92 75

Neomeris (38) 48 (45) 25 21 (31) 33 50 30

Rhipidosiphon 25

Trichosolen

Tydemania

Udotea 58 (58)

Valonia

Ventricaria 25

Red algae

Acanthophora

Actinotrichia

Amansia

Amphiroa (48) (29) (42) 50 (36)

Asparagopsis 50

Botryocladia

Cheilosporum

Chondria

Coelarthum

Crouania

Dasya

Galaxaura 33 (37) 25 (24) 25

Gelid 92 38

Gracilaria

Halychrysis

Hypnea

Jania (30.6) (27.8) (45.0) (52.8) (63.9) (44.4)

Laurencia/ch (38) 42

Liagora (25)

Martensia

Peyssonnelia (33)

Porteiria

Tricleocarpa 50

Wrangelia

Yamadaella

Brown algae

Dictyota (44) 38 (39) (29) (28) (20) (25) 50 (36)

Lobophora 42 83 (81) 75 (78) 40 (36) 71 (78)

Padina 58 (25) 25

Turbinaria 25

192 Phycologia, Vol. 46 (2), 2007

Table 3. Two-way nested ANOSIM: r values among islands and sites in 2003 and 2005. Each r value had a P value 0.001.

Comp 2003/200*-****-****

46 common sites assessed 46 common sites assessed

All 64 sites sampled in 2003 and 2005 All 70 sites sampled in 2003 and 2005

Islands 0.22 (n 15) 0.28 (n 13) 0.25 (n 16) 0.29 (n 13)

Sites 0.41 0.35 0.40 0.41

0.29, P 0.001) and moderate differences among sites within other end of the ordination. Islands that did not follow geo-

islands (r values 0.35, 0.41, P 0.001). graphic trends in the nMDS ordination include the volcanic

Relationships among islands based on RAM were illustrated island Pagan, whose algal ora was more similar to Saipan and

using nonmetric multidimensional scaling (nMDS) (Fig. 3). The Tinian than other northern islands, and Alamagan and Guguan,

nMDS clustered Santa Rosa, Guam, Rota, Aguijan, Tinian, and whose algal oras were more closely aligned to the southern

Saipan together at one end of the ordination, similar to their island of Aguijan. Finally, Anatahan was situated with the

geographic location at the southern end of the Archipelago (Fig. northernmost islands in the nMDS ordination (close to Uracas).

1). Similarly, most volcanic islands clustered together at the Stress values of 0.09 and 0.1 in 2003 and 2005, respectively,

indicate a good representation of island relationships in the two-

dimensional nMDS ordinations based on RAM (Chapman &

Underwood 1999). Because relationships of islands in the

nMDS ordinations were similar regardless of sampling year,

only the nMDS map for 2003 is presented (Fig. 3).

Temporal variability

The two-way crossed ANOSIM comparing years and sites across

the Mariana Archipelago showed differences in RAM among

sites (r value 0.52, P 0.001) and moderate differences over

time (r value 0.39, P 0.001; Clarke & Warwick 2001).

Island by island, the two-way crossed ANOSIMs showed similar

moderate changes of RAM between 2003 and 2005 (r values

0.28 0.39, P 0.001) except for Agrihan, Sarigan, Tinian, Rota,

Guam, and Santa Rosa, where the change was more statistically

signi cant (r values 0.43 0.57, P 0.001, Table 4). Aguijan

was the only island at which RAM did not change over time (r

value 0.18, P 0.001). The two-way crossed ANOSIMs also

highlighted a higher variability of RAM among sites at the south-

ern carbonate islands (average r value 0.48) than at the vol-

canic islands (average r value 0.28, P 0.001; Table 4). No

change in RAM was observed among sites at Uracas, Asuncion,

and Sarigan.

DISCUSSION

This study provides the rst quantitative data of algal genera

and functional groups across the entire Mariana Archipelago

and lays the groundwork for continued algal monitoring stud-

ies. It also represents the second major collection of macroal-

gal genera from the northernmost Mariana Islands. All 47 gen-

era found had been previously reported for the archipelago

(Tsuda & Tobias 1977a, b; Tsuda 2003), and many new spe-

cies records from these collections are in the process of being

documented (R. Tsuda, personal communication).

Spatial variability

As documented in the Hawaiian Archipelago (Vroom et al.

2005a; Vroom & Page 2006), habitat variability within single

island ecosystems can vary dramatically depending on oceano-

Fig. 3. nMDS plot mapping relationships among islands based on

graphic conditions, geomorphology, and island size. In the Mar-

average genus ranks in 2003. Stress 0.09. Island abbreviations are

iana Archipelago, the northern volcanic islands contain often

listed in Appendix 1. Squares represent southern carbonate islands;

poorly developed, steep reefs composed of massive boulders or

triangles represent northern volcanic islands.

Tribollet & Vroom: Macroalgae of the Mariana Islands 193

Table 4. Two-way crossed ANOSIM: r values between years and among sites within individual islands. n number of common sites visited

at each island in 2003 and 2005. Each r value had a P value 0.001.

Santa

Island Rosa Guam Rota Aguijan Tinian Saipan Sarigan Alamagan Pagan Agrihan Asuncion Maug Uracas

r-values (n 1) (n 6) (n 5) (n 2) (n 3) (n 3) (n 2) (n 3) (n 6) (n 3) (n 3) (n 7) (n 3)

Years 0.49 0.46 0.43 0.18 0.47 0.34 0.57 0.38 0.36 0.46 0.39 0.32 0.28

Sites xx 0.44 0.61 0.25 0.36 0.72 0.13 0.4 0.29 0.34 0.24 0.37 0.21

large plains of black sand, although some of the larger islands lands (Fig. 2), especially during winter months. A similar

exhibit calmer lagoon-like or reef at areas. Southern carbonate trend has been observed in the subtropical Northwestern Ha-

islands contain broader reef ats or shallow regions that typically waiian Islands (Vroom & Page 2006), and brown algae are

extend 1 km from shore, providing considerably more reef known to predominate over other algal lineages in cool, tem-

heterogeneity than at northern locales. Thus, it is not surprising perate environments (Cheney 1977).

that the two-way crossed ANOSIM revealed that larger islands, In addition to anthropogenic activities and oceanographic con-

containing greater habitat diversity, exhibited higher diversity ditions discussed above, feral animals, weather conditions (e.g.

among sites than smaller islands. However, in nMDS ordinations, storms, typhoons), and volcanic eruptions can also in uence spa-

Pagan (the largest of the northern, volcanic islands) clusters tial variability observed across the archipelago. In the past four

closely to the southern, carbonate islands because its larger size years, the southern islands were affected by more typhoons than

likely allows for higher generic macroalgal diversity (23 genera the northern islands (Table 1), although Alamagan, Pagan, and

and ve functional groups). Similarly, although Maug has a sur- Agrihan also experienced severe storm activity. Such weather

face area of only 2 km2, it also clusters close to larger islands conditions may be responsible for the high variability in RAM

because its unique geomorphology (three small islets surrounding between sites at the latter three islands (Vroom et al. 2005b). On

a large ooded caldera) allows for a wider variety of habitats islands experiencing volcanic activity, reefs are heavily impacted.

and, accordingly, relatively high algal richness (22 genera and The northern side of Anatahan Island was surveyed four months

four functional groups). Habitat differences make each island after its violent eruption on 10 May 2003 (Wiens et al. 2004),

unique, and higher abundance of certain algae over others at each and the reefs were found buried in silt-like ash, reducing the

island is re ected through RAM. Two-way nested ANOSIMs visibility to less than 0.5 m. By contrast, southern and western

revealed moderate differences in RAM when all sites surveyed reefs of Anatahan were clearer, probably because of lighter ash

across the archipelago were considered simultaneously. Such re- fall and higher wave energy, clearing away ash deposits. Surveys

sults are expected as algal genus composition changes from hab- conducted at Anatahan found algal populations to have suffered

itat to habitat within a single island ecosystem (e.g. wave-ex- as a result of the eruption. For instance, substantially fewer mac-

posed fore-reefs vs calm lagoonal reefs; Vroom et al. 2005a). roscopic algal genera occurred on Anatahan (seven genera and

The nMDS plot generated using RAM for each island close- three functional groups) than on geographically close islands

ly resembled a geographical map of the Mariana Archipelago. (Sarigan and Saipan with 13 to 25 genera and ve functional

This con rmed that detectable differences in genus presence groups), and populations of algae present were much smaller.

and rank exist among islands and mirrored geographic rela- These differences were re ected by the placement of Anatahan

tionships (Figs 1, 2). Rapid ecological algal assessments using away from geographically close islands in the nMDS plot but

data from the Northwestern Hawaiian Islands (Vroom & Page fairly close to Uracas. Uracas is the smallest and newest island

2006) revealed a similar trend between geographic orientation in the Mariana Archipelago (Bearden et al. 2005) and has erupt-

and relationships among islands based on RAM. In this study, ed at least 16 times in the past 150 years (Uracas 2006). It is

turf algae, crustose coralline red algae, and the green algal hypothesized that the low macroalgal diversity (nine genera plus

genus Halimeda were ubiquitous across the archipelago, a two functional groups) recorded at Uracas during our expeditions

nding in line with similar studies of US coral reefs across is due to its continually developing reef systems.

the Paci c (Adey 1998; National Marine Fisheries Service

2004, 2005; Vroom et al. 2005a; Vroom & Page 2006). Yet Temporal variability

despite the relative homogeneity of macroalgal genera across

Storm, anthropogenic, and volcanic activities not only in u-

the archipelago, southern islands can be distinguished from

enced the spatial variability of RAM but also likely accounted

the northern islands based on generic composition. For in-

for some temporal changes observed in the Mariana Archi-

stance, Dictyosphaeria and cyanophytes were encountered

pelago between the 2003 to 2005 surveys. Between our two

more frequently in southern than northern islands, and differ-

research expeditions, ve typhoons swept over various islands

ences in RAM among sites were more pronounced in southern

in Guam and CNMI. Recent research on the effects of severe

islands, a pattern that may result from localized anthropogenic

storms on algal populations (Vroom et al. 2005b) found that

activity in southern islands such as Guam (e.g. eutrophication,

substrata can be scoured clean by severe wave energy and that

pollution; Thacker et al. 2001; see Table 2 for human popu-

certain genera fare better than others at re-establishing popu-

lation densities across the archipelago). Cyanophytes and the

lations (McManus & Polsenberg 2004). Therefore, it is not

genus Dictyosphaeria are often abundant in eutrophic and

surprising that the islands situated closest to the path of the

heavily shed reef areas (Adey 1998; Larned 1998; LeBris et

storms (Guam, Rota, Tinian, Saipan, Santa Rosa, Agrihan, and

al. 1998; Stimson et al. 2001). In contrast, the frequency of

Sarigan) exhibited the highest degree of temporal difference

the phaeophyte Lobophora in the northern islands may be re-

lated to cooler sea surface temperatures found in northern is- in RAM. Sarigan, the island exhibiting the highest degree of

194 Phycologia, Vol. 46 (2), 2007

ity affects algal functional community dynamics by clearing

temporal change in our study, might also have been affected

space for opportunistic species to settle and grow (McManus

by the volcanic eruptions of Anatahan in 2003 and 2005. Sur-

& Polsenberg 2004).

veys at Sarigan (the closest neighbor to Anatahan) in 2003

When spatial variability of RAM was considered, the

revealed a thin layer of ash over large areas of reef that was

NWHI and Mariana archipelagoes exhibited opposite trends.

absent at other islands (Bearden et al. 2005).

In the NWHI, most island comparisons yielded negative r val-

Temporal variability in RAM at southern islands may also

ues, whereas island comparisons in the Mariana Archipelago

be related to the intensity and nature of human activities (see

exhibited positive r values. This indicates that, in the NWHI,

Table 2 for human population densities across the archipela-

more variability exists within reef ecosystems surrounding

go). Although Abraham et al. (2004) reported little change in

each island than among islands as a whole (Vroom & Page

coral and macroinvertebrate communities in CNMI between

2006). In the Mariana Archipelago, positive r values among

2002 and 2004, he suggested that polluted runoff from areas

sites revealed a relative homogeneity within each island eco-

of high population density and increases in shing pressure in

system surveyed. These differences likely occur because the

Guam are increasingly degrading coral reef ecosystems and

NWHI are estimated to be 75 million years (myr) old (Clague

slowing reef recovery after natural disturbances such as ty-

& Dalrymphe 1987; Kim et al. 1998) and are the remains of

phoons. Therefore, it is not surprising that the unpopulated

larger islands that have slowly sunk over time, allowing myr-

island of Aguijan (Table 4) was the only southern carbonate

iad habitat types to have evolved within the geologically com-

island not to exhibit temporal changes in RAM, even though

plex reef shelves found at each atoll or island. In comparison,

it experienced typhoon and storm activity similar to Rota and

the Mariana Archipelago is as young as 55 to 20 myr (Meijer

Guam. Because of less anthropogenic disturbance, Aguijan

et al. 1983; Stafford et al. 2005), with many islands still con-

also continues to exhibit extensive coral growth (Abraham et

sisting of active volcanoes whose eruptions limit habitat var-

al. 2004). Based on our analyses, anthropogenic impacts (in-

iability and continue to dramatically impact the reef environ-

cluding shing, sedimentation, and eutrophication), combined

ment. The northernmost Mariana Islands slope steeply to great

with storm damage, appear to be a major factor affecting

depths with little room for complex reef development and ac-

RAM on tropical reefs located at the southern end of the ar-

cordingly contain young reefs with relatively low algal diver-

chipelago. This lends further support to Hallock s (2005) sug-

sity compared to older ecosystems. Additionally, the NWHI

gestion that hurricane impacts on coastal ecosystems are ex-

chain is much longer (2600 km) than the Mariana Archipelago

acerbated by deforestation, agriculture, and coastal develop-

(750 km) and experiences higher annual uctuations in sea

ment. On the northern islands experiencing volcanic activity,

surface temperature (Bearden et al. 2005; Friedlander et al.

reefs are constantly being rebuilt. Surveys conducted at south-

2005). Such temperature variations play an important role in

ern and western sites of Anatahan found algal populations to

algal diversity, abundance, and distribution (Cheney 1977;

have suffered as a result of the May 2003 eruption (Bearden

Adey 1998; Thacker et al. 2001).

et al. 2005), with existing algal turf communities trapping ash,

This study suggests that RAM has high potential as a tool

leading to subsequent decreased light-absorbing and nutrient-

to rapidly assess changes in coral reef communities, both spa-

uptake capabilities by these turf algal communities (Irving &

tially and temporally. In the Mariana Archipelago, geomor-

Connell 2002). Thus, turf communities were reduced up to

phology is likely to be the principal factor that affects RAM

50% when compared to neighboring islands (personal obser-

spatially, although anthropogenic, storm, and volcanic activi-

vation). Anatahan provides a unique opportunity to observe

ties likely play secondary roles in structuring algal commu-

recovery and development of reef communities including ma-

nities. The degree of temporal variability observed across the

croalgae over the next several decades.

archipelago within a two-year period was surprising because

both assessments occurred during the same seasonal time

Comparisons to the Northwestern Hawaiian Islands

frame. We hypothesize that temporal variation in algal com-

An analysis similar to our study of the Mariana Archipelago munities, like patterns of spatial variability, occurred because

was recently completed for the Northwestern Hawaiian Is- of the combined effects of typhoon intensity and frequency,

lands (NWHI; Vroom & Page 2006) and reveals enlightening volcanic eruptions, and human activities. The degree of tem-

differences between the two archipelagoes. Temporal vari- poral variation observed in the Mariana Archipelago differed

ability of RAM across the NWHI as a whole was not signif- from the NWHI, where RAM varied more spatially than tem-

icant despite known temperature variations over latitudes porally. Differences between the two archipelagoes include

(Bearden et al. 2005) but was moderately signi cant in the less human pressure, larger and more complex islands, in-

Mariana Archipelago, where temperature variations are rela- creased age of the archipelago, as well as greater uctuation

tively small. It is hypothesized that differences between these of oceanographic conditions (such as sea surface temperature)

two Paci c archipelagoes are attributable primarily to natural in the NWHI than in the Mariana Archipelago. The continued

environmental pressures (severe typhoon damage and volcanic use of the Preskitt method (Preskitt et al. 2004) to rank ma-

activity) coupled with higher anthropogenic activities in the croalgal genera in island systems around the Paci c (Vroom

Mariana Archipelago and limited environmental pressures or et al. 2005a, 2006; Vroom & Page 2006) will provide com-

human activities in the mostly unpopulated NWHI. Despite plementary data on macroalgal diversity, abundance, and dis-

the relatively pristine nature of the NWHI, moderate temporal tribution from other island systems. Additionally, long-term

variability was seen in the three northernmost atolls of NWHI surveys using the technique discussed here, combined with

when they are considered separately from the entire archipel- future detailed species-level analyses, are necessary in order

ago because of two mass coral-bleaching events in 2002 and to con rm the trends observed over a two-year period and to

sort out which environmental factors or anthropogenic activ-

2004 (Vroom & Page 2006). Increasing substratum availabil-

Tribollet & Vroom: Macroalgae of the Mariana Islands 195

and Paci c Freely Associated States: 2005 (Ed. by J.E. Waddell),

ities in uence RAM most heavily. Such surveys will allow

pp. 270 311. NOAA Technical Memorandum NOS NCCOS 11.

better management of coral reefs, especially those impacted

NOAA/NCCOS Center for Coastal Monitoring and Assessment s

by human activities.

Biogeography Team, Silver Spring, MD. 522 pp.

GATTUSO, J.-P., M. FRANKIGNOULLE, S.V. SMITH, J.R. WARE, R. WOL-

LAST, R.W. BUDDEMEIER & H. KAYANNE. 1996a. Coral reefs and

ACKNOWLEDGEMENTS

carbon dioxide. Science 271: 1298 1300.

GATTUSO J.-P., PICHON M., DELESALLE B., CANON C. & FRANKIGNOULLE

We thank Kimberly Page (CRED), Elizabeth Keenan (CRED), M. 1996b. Carbon uxes in coral reefs. I. Lagrangian measurement

Fran Castro (CMNI Department of Environmental Quality), and of community metabolism and resulting air-sea CO2 disequilibrium.

Marine Ecology Progress Series 145: 109 121.

Shawn Wusstig (Guam Division of Aquatic and Wildlife Re-

GATTUSO J.-P., PAYRI C.E., PICHON M., DELESALLE B. & FRANKIG-

sources) for their help collecting algal eld data as well as all

NOULLE M. 1997. Primary production, calci cation, and air-sea CO2

other members of the CNMI and Guam benthic teams. Special

uxes of a macroalgal-dominated coral reef community (Moorea,

thanks to Captains Ken Barton and Mike Devany, our benthic French Polynesia). Journal of Phycology 33: 729 738.

coxswains Bruce Mokiao and Ariana Lynn, and the rest of the GILMAN E.L. 1997. A method to investigate wetland mitigation bank-

crew of the Oscar Elton Sette. Funding to PIFSC-CRED for ing for Saipan, Commonwealth of the Northern Mariana Islands.

scienti c expeditions to the Mariana Archipelago was provided Ocean and Coastal Management 34: 117 152.

GORDON G.D., MASAKI T. & AKIOKA H. 1976. Floristic and distribu-

through the NOAA Fisheries Of ce of Habitat Conservation as

tional account of the common crustose coralline algae on Guam.

part of the NOAA Coral Reef Conservation Program.

Micronesia. 12: 247 277.

HALLOCK P. 2005. Global change and modern coral reefs: new oppor-

tunities to understand shallow water carbonate depositional pro-

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