Reefs That Rock and Roll: Biology and ...

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REEFS THAT ROCK AND ROLL: BIOLOGY AND CONSERVATION OF RHODOLITH BEDS IN THE GULF OF CALIFORNIA

RAFAEL RIOSMENA‐RODRIGUEZ, DIANA L. STELLER, GUSTAVO HINOJOSA‐ARANGO AND MICHAEL S. FOSTER

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Edited

by Richard C. Brusca

Foreword

by Rodrigo A. Medellin

Edited by Richard C. Brusca

The University of Arizona Press and The Arizona-Sonora Desert Museum

I Tucson

Arizona-Sonora Desert museum Studies SERIES EDITORS

Richard C. Brusca, Ph.D. Christlne Come, Ph.D. Mark A. Dimmit, Ph.D.

The University of Arizona Press

漏 2010 The Arizona Board of Regents All rights reserved www.uapress.arizona.edu Library of Congress Cataloging-in-Publication Data

The Gulf of California : biodiversity and conservation / Rich

p. cm.

Includes bibliographical references and index.

1.

Biodiversity-Mexico- California, Gulf of.

2.

Wildlife

Gulf of. 3. Natural history - Mexico-California, Gulf of. 1 QH95-4-G852010

508 路3 164' I-dC22

o

Manufactured in the United States of America on acid-free, a

quality paper containing a minimum of 30 percent post-consu waste and processed chlorine free.

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14

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2

Introduction RICHARD C. BRUSCA

1

Origin, Age, and Geological Evolution of the Gulf of California

7

JORGE LEDESMA-VAZQUEZ AND ANA LUISA CARRENO

2

Physical, Chemical, and Biological Oceanognphy of the Gulf of California

24

SAUL ALVAREZ-BORREGO

3

Reefs That Rock and Roll: Biology and Conservation of Rhodolith Beds in the Gulf of California

49

RAFAEL RIOSMENA-RODRIGUEZ, DIANA L. STELLER, GUSTAVO HI NOJOSA-ARANGO, AND MICHAEL S. FOSTER

4

Invertebrate Biodiversity and Conservation in the Gulf of California

72

RICHARD C. BRUSCA AND MICHEL E. HENDRICKX

5

Fishes of the Gulf of California

96

PHILIP A. HASTINGS, LLOYD T. FINDLEY, AND ALBERT M. VAN DER H EIDEN

6

The Importance of Fisheries in the Gulf of California and Ecosystem-Based Sustainable Co-Manag'ement for Conservation

119

MIGUEL A. CISNERO S-MA TA

viii I

CONTENTS

7

Sea Turtles of the Gulf of California and Conservation 135 JEFFREY A. SEMINOFF

8

Ospreys of the Gulf of California: Ec Conservation Status 168 jEAN-LUC E. CARTRON, DANIEL W.

CHARLES j. HENNY, AND ROBERTO C

9

Marine Mammals of the Gulf of Cali

An Overview of Diversity and Conse JORGE URBAN R.

10 A Brief Natural History of Algae in t RICHARD MCCOURT

11 Ecological Conservation in the Gulf o MARIA DE LOS ANGELES CARVAJAL, AND EXEQUIEL EZCURRA

Bibliography

251

About the Contributors Index

337

33 I

STELLER, GUSTAVO HINOJOSA-ARANGO, AND MICHAEL S. FOSTER

Introduction

I

magine an underwater field of closely packed, purple-pink sphere about the size of golf balls, each composed of numerous calcareous branche radiating out from the center of the sphere. The spheres and hundreds o species of animals and seaweeds living on and in them move with the mo

tion of waves and currents. These spheres are rhodoliths, and beds of thes calcareous red algal spheres comprise a rarely mentioned but common habi tat in global nearshore environments. Rhodoliths are not generally include in natural history and diving guides. The rhodoliths themselves are attrac

tive because of their color and range of morphologies and because of th variety of organisms associated with the beds. Local people view rhodo lith beds in terms of the associated rich fisheries or as recruitment sites fo harvestable species.

Rhodoliths are morphologically diverse, free-living, non geniculate coralline red algae (Rhodophyta: Corallinales) that form extensive living beds worldwide (color plate 2A) and are abundant in fossil deposits from theearly Cretaceous to the Pleistocene (Aguirre et al. 2000; Foster 2001) . As

with many attached reef-forming coralline species (Steneck and Adey 1976) rhodolith size, shape, and branching vary among species and-primarily as a result of variation in water motion-within species (Bosence 1976; Foste et al. 1997). Much like the maerl beds common to the northeastern Atlantic, rhodolith beds are benthic communities dominated by rhodoliths

50/ RIOSMENA-RODRfGUEZ ET AL .

that collectively create a fragile, structure This matrix provides habitat for diverse

algae (Cabioch 1969; Keegan 1974; Bosen unusual, and endemic species in rhodoli

geographically diverse locations includin

Grave 1999), Norwegian fjords (Freiwald (Ballesteros 1988), the tropical Atlantic ( Ocean (Weber-Van Bosse and Foslie 1904 ical and subtropical Pacific, including the

et at. 1997; Clark 2000; James et at. zo06; Living rhodoliths occur as an up rounded thalli that overlay carbonate sedi are often the result oflong-term accumul

parts from other calcified organisms such

and Nakamori 198z; Steller and Foster 1 In the northeastern Atlantic, unconsolid

been harvested for a variety of human use

and in many other locations the beds are

(B1unden et at. 1977; Briand 1991; revie studies in the northeastern Atlantic and these common benthic environments are n

caused by harvesting (Blunden et at. 19

Spencer and Moore zooo; Bordehore et from activities that reduce water quality

tion (Blunden et at. 1981; Hily et at. 199z growth rates (review in Foster ZOOI; Stell negative impacts of burial make rhodolith disturbance and extraction (Adey and M These community attributes have led to t

as threatened and protected in New Zeala

1998), Australian (Director of National Pa

et at. 1998) coastal habitats.

Rhodoliths in the Gulf of Califo

since the late 1880s (Hariot 189S), but th and living beds (fig. 3.1) dominated by th importance to nearshore ecology, and the

D "

38'0

d.

3.1. Known locations ofliving rhodolith beds in the Gulf of California, A rhodolith bed consists of an area of 10% or greater cover of rhodoliths. All beds except those designated E,Y D (E, Yale Dawson; Dawson 1960b) or 0 (other) were observed by one or more of the authors (contact the authors for details).

Dawson's observations were based on dredged material or were not specified, Numbers correspond to following sites by region. Puerto Penasco/Guay mas Region: (I) Punta Borrascosa (0); (2) Manto Penasco (0); (3) Estero Morua (0) (4) Cabo Tepoca; (5) Estero Arenas (0); (6) Estero Santa Rosa; (7) Isla Alcatraz; (8) Isla San Pedro Martir (0); (9) Isla San Pedro de Nolasco; (10) Las Gringas; and (II) Bahia Bocochibampo (E.YD.). Bahia de los Angeles Region: (12) Isla Partida (E.YD .); (13) Puerto Refugio (0); (14) Canal Mejia (0); (15) Isla Cabez de Caballo; (16) Bahia de San Francisco Pond Island (E.YD" 0); (17) Bahia de Palomas (0); (18) Punta Chivato I; and (19) Punta Chivato II , Bahia Concepcion Region: (20) Punta Aguja (Concepcion, E.YD,); (21) Los Machos; (22) Santisp (23) Isla Blanca; (24) Isla Coyote; (25) Morro Tecomates; (26) EI Cardon; (27) I EI Requeson; (28) La Cueva (Correcaminos); (29) Los Pocitos; and (30) EI Coloradito, Loreto Region: (31) Punta Bajo; (32) Isla Coronado Channel; (33) Is Coronado; (34) Isla Carmen (in Bahia Salinas, E.YD" 0); (35) Isla Danzante (0 (36) Puerto Escondido (EYD.); (37) Islas Las Galleras; (38) Isla Catalina (0); (39) Isla Santa Cruz (EYD .); (40) Isla San Diego; (41) Isla San Jose; (42) Isla S Jose Estero; (43) Isla El Pardito; (44) La Lobera; and (45) Isla San Francisquito, La Paz Region: (46) Los Islotes (0); (47) Bahia San Gabriel; (48) Canal de San Lorenzo; (49) Punta Galeras; (50) Isla Gaviota; (51) Bahia de La Paz (Malecon/ historic site, E.YD., 0); (52) Isla Cerralvo (0); (53) Punta Perico; (54) Cabo Pulmo (0); and (55) Bajo La Gorda (EYD ,), Sinaloa Region: (56) Topolobamp (EYD.) and (57) Isla Venado. Nayarit Region: (58) Isla Isabel (0); (59) Isla Ma (0); and (60) Isla Marietas. Note that beds 57-60 are off the map (to the south)

52/ RIOSMENA-RODRfGUEZ ET AL.

Gulfwas not appreciated until the early 19 Our purpose is to review what is known California and then to discuss this inform as it concerns their present and future con

Spatial Distribution of Uuing

When compared with kelp forest major communities dominated by macrop is poorly known. This is because beds are surface, commonly occur in areas though can shift in location. The world distributi from that of Bosence (1983), shows that widespread from polar regions to the trop the northwestern Atlantic, Caribbean, Gu Shelf and Western Australia. Such a distr rence of rhodolith beds is probably not d

variation in temperature, mean solar inpu It has been argued by Halfar et a the Gulf of California promote the grow et al. (Z004b) sampled four sites from Ca geles in finding rhodoliths most abundan sotrophic" sites, suggesting support for n Halfar and Mutti (zo05) argued that inc partly responsible for shifts from coral t the Miocene. However, the core of this a

general or rhodoliths in particular devel nutrient conditions-may be an artifact sampled at each site. Extensive rhodolith

et al.'s southern, "oligo-mesotrophic" site fig. 3.1), and at their northern, "eutroph (Dawson 1960b; fig. 3.1). Moreover, it is w dant invertebrate assemblages occur wit Such dense faunal assemblages are capabl cally contribute to macroalgal growth (Br duced by the rhodolith bed fauna, in conju

It may be that coral formations can dominate rhodoliths for space in su

situations (at least in shallow water) as suggested by the rhodolith and cor

sequences in cores from some coral reefs (Payri and Cabioch 2004) .

It follows from these observations that local, not latitudinal, e vironmental variation has the greatest effects on the presence and pers

tence of rhodolith beds. This suggests that-except in high-temperatur

low-nutrient tropical environments, where rhodoliths might lose to cora

in the competition for space-using the presence (or absence) of livi

rhodolith beds or rhodolithsin the fossil record to intuit broadscale d

ferences in present or historical environments can be misleading. At loc scales, the consensus is that rhodoliths need to be moved to be maintain

in a free-living state, and this movement is driven by water motion an

bioturbation (reviews in Bosence 1983; Foster 2001). Water motion also r

duces the probability of burial by inhibiting sedimentation of fine particl

and resuspending such particles after periods of low water motion (Stell and Foster 1995; Marrack 1999; Mitchell and Collins 2004). However, hi water motion may break the thalli, especially of delicate species such

Lithophyllum margaritae (Steller and Foster 1995), or transport thalli in

habitats unfavorable for growth. Distributional data suggest that rhodoli

beds generally occur on flat to gently sloping soft bottoms, where rhod Ii ths and free-Ii ving forms of other organisms (such as corals and bryozoan

Reyes-Bonilla et al. 1997; James et al. 2006) can accumulate and where lig is sufficient for rhodolith growth.

In the Gulf of California, rhodolith beds have consistently be

found at semi-protected (from waves) sites around islands and in bays, an

in channels, from north of Puerto Penasco, Sonora, to Islas Marietas, Jalis

(fig. 3. I). This distribution should be considered tentative, since intensi

surveys have only been done in the region around La Paz and Mulege. Th

54/

RIOSMENA-RODRiGUEZ ET AL.

shoreline extent and depth of most of thes however, occur in one of two general types dominant water conditions. Wave beds gro 12 m) on gently sloping soft bottoms expos beds 22-30 in fig . 3.1); current beds general

on relatively flat bottoms exposed to tidal c in fig. 3.1). In wave beds, the water motion rhodoliths and inhibit the accumulation o the large-scale sediment is transported d pers. obs.); it may be that bioturbation ca that currents inhibit the accumulation of these categories is a tidally driven "current estuary (bed 6 in fig. 3.1). At present it is u Massive bed relocation as well as water can occur during episodic events suc

been observed after hurricanes (M . Foster pers. obs.), and the latter is indicated by la fragments in sediment cores from depths

large bed (bed 48 in fig. 3.1) in Canal de Sa son 1969; Foster, pers . obs.). The lower lim termined by sedimentation (Steller and Fo bed found to date is 35-40 m at Punta Per Elizondo 2005). In areas where suitable su likely that the lower limits of such beds are may thus have an indirect effect on the dep light via effects on phytoplankton biomass.

These constraints, whose existenc suggest that any larger-scale distribution p ferences in nearshore geomorphology, wate conclusion similar to Nelson's ill: his review (Nelson 1988). The abundance of rhodoli variation in rhodolith growth rates due to calcium carbonate. The great variation in t composition found within a local site (e.g., 1997; Halfar et al. 2000a) argues for caution ter sampling only a few localized modern b

traditional SCUBA sampling and continuous, bed-scale in situ recordi

of appropriate environmental variables (e.g., Mitchell and Collins Z00

will provide the descriptive information necessary to develop more rigoro hypotheses that can be experimentally tested.

Taxonomic Oiuersity of Rhodoliths

One of the major problems in working with rhodoliths and coralli

algae in general is the identification of specimens to the generic or speci

level. The classification within this order has changed from the recogniti

of one or two families (Corallinaceae and Solenoporaceae) in the early twe

tieth century to the recognition of three families (Corallinaceae, Hapalid ceae, and Sporolithaceae) at the beginning of the twenty-first century (Ha

vey et al. 2003). The changes have been more dramatic at the generic lev

and a major evaluation (Woelkerling I988) was necessary to settle many the classical problems. However, boundaries of genera and species remain

common problem best solved by regional monographs using consistent d

agnostic features (Riosmena-Rodriguez et a!. I999; Harvey et a!. Z003). O

of the major problems is that many growth-forms can occur in the sam

species (Woelkerling et al. I993; Riosmena-Rodriguez et a!. 1999).

Riosmena-Rodriguez et a!. (I999), Riosmena-Rodriguez (200Z), a Vazquez-Elizondo (2005) based their taxonomic surveys on specimens fro

55 localities, identifying four main rhodolith species in the Gulf of Califo

nia: Lithophyllum margaritae (fig. 3.z) as well as Neogoniolithon trichotomu

Mesophyllum engelhartii, and Lithothamnion muellerii (= Lithothamniu

crassiusculum) (resp. fig. 3.3A, B, C). There may be a fifth species, dependi on the pending taxonomic resolution of Lithothamnion australe (Riosmen

Rodriguez 200Z). Additional species in the genera Archeolithothamnium an

Lithothamnion have been recorded from Eocene deposits (Durham 195

r

56/

RIOSMENA-RODRiGUEZ ET AL.

3.2. Growth-form variation in Lithophyllum mar

(right) to fruticose (left top) to lumpy (left cente center. From Riosmena-Rodriguez et al. (1999);

Squires and Demetrion 1992; Abbott et a

ment because Archeolithothamnium is a hete

(Woelkerling 1988), which means that confir

tion is required before species can be determ

scriptions for the abundant rhodoliths from P

Foster et al. 1997; Cintra-Buenrostro et al. 2

graph on these is needed to determine the sp

3.3. Other rhodolith-forming species from the GulfofCalifornia with less variabl

growth-forms than Lithophyllum margaritae. (A) Neogoniolithon tl"ichotomum: specimen with fruticose growth-form; scale bar = I cm. (B) Mesophyllum engelhartii: specimen with fruticose growth-form; scale bar = I cm. (C) Lithothamnion muellerii: specimens with fruticose to lumpy growth-forms; scale bar = 3 cm.

cies in the fossil record. Such a monograph would also facilitate stratigrap analyses and the interpretation of historic changes in distribution.

Modern taxonomic approaches based on careful evaluation of a

tomical structures (Harvey and Woelkerling 2007) combined with molec

lar analysis as described in Harvey et al. (2003) are crucial to rigorous ide

tification. Assessment of anatomical structures requires thin histologi

sections, especially of the pore area over conceptacles, in addition to opti and scanning electron microscopy (SEM; Woelkerling 1988; Riosme

Rodriguez et al. 1999). The main features used to distinguish species

the Gulf are used in the key (table 3.1) and illustrated in figure 3+ T

primary structures that must be assessed are whether the epithelial ce . are flared or flat/rounded, the kind of interfilament connections pres

r

58/

RIOsMENA-RODRIGUEZ ET AL.

Tft8LE 3.1. Taxonomic key to rhodolit

(terminology based on Woelkerling 19 I

a. Foliose to fruticose growth form, thalli connected with secondary pit connectio (fig. 3-4C) present. Epithelial cells flat/ flared (fig. 3-4B). Uniporate tetrasporan

I

b. Lumpy to fruticase to incrusting grow filaments connected and cell fusions pr rounded. Multiporate tetrasporangial c

2a. Foliose to fruticose growth-form , thalli nected but only secondary pit connectio absent.

2b. Fruticose growth-form and only celJ fu Neogonio

3a. Lumpy to fruticose growth-form, flared (fig. 3-4B).

3b. Fruticose to incrusting路 growth-form, ro subepithelial cell.

(no evident connections, secondary p and "vhether the tetrasporangial conc Further molecular analyses are being

cies limits in the Gulf (Riosmena-Ro All the recognized species ar gal'itae is especially so: individuals m

lumpy growth-forms or may exhibit species is widely distributed in the

Gulf. The morphology of the other

and fruticose (fig. 3.3A-C). Lithotha cur only in the most wave-exposed, s sediment among rocks and Sargassu

Gulf. Neogoniolithon trichotomum (fig are well protected from waves. It is

has not been found deeper than 12 has only been found in bed 53 (fig. 3. rhodolith-forming species is higher

3.4. Main anatomical features

used to identify rhodolith-forming species.

(A) Longitudinal section showing the flat/rounded epithelial cells (black arrow) and secondary pit connections (white arrow); scale bar = 10 mm.

(B) Longitudinal section showing flared epithelial cells (arrow); scale bar = 10 mm. (C) Longitudinal fracture showing cell fusions (arrow); scale bar = IO mm. (D) Longitudinal section of a uniporate tetrasporangial conceptacie (arrow); scale bar = 100 mm . (E) Longitudinal section of a tetrasporangial conceptacie with a multiporate roof (arrows); scale bar = 100 mm.

geographic regions (with the exception of the northeastern Atlantic an

Mediterranean). For example, there is only one species in the temperat northwestern Atlantic (Bird and McLachlan 199z) and three in the tropica northwestern Atlantic (Littler and Littler zooo) . There are twelve specie

in the northeastern Atlantic (Cabioch et al. 199z; Irvine and Chamberlai 1994) and four species in the Mediterranean (Cabioch et al. 199z; Bordehor et al. zooz); the Indian Ocean hosts three species (Verheij 1993), the wester Pacific two species (Woelkerling 1996a-e; Littler and Littler zo03), and th temperate northeastern Pacific three species (Athanasiadis et al. Z004).

Rhodolith morphology and Growth

Rhodolith morphology varies depending on the growth environ ment (Bossellini and Ginsburg 1971; review in Bosence 1983). In the Gulf

60 / RIOSMENA-RODRIGUEZ ET AL.

individual Lithophyllum margaritae rhodoli

spherical, and have higher branch densities a

and Foster 1995; Foster et al. 1997). Althou

ter motion, there is little evidence that lig

in morphology, including' that between wav

fluenced genetic exchange among rhodolith

thereby resulted in geographic isolation (Sch

is no doubt also influenced by veg'etative rep

rhodoliths appear to grow from fragments. R pear to result from the interplay between th

Individual rhodoliths may origin spores, or coralline alg'al fragments broken f

shells (reviewed in Foster ZOOI). Regardless Iiths have persistent growth bands along' the

vital stains. Rivera et al. (zo04), using field a

southern Gulfwith L. muellerii (= L. cras

found an average growth rate of 0.6 mm / yr,

duced annually, and that the number of ban

lated to branch length , This relationship wa

of the largest L. muellerii collected (~I 5 cm)

verified for L. muelleri from the same bed by

timing of variation in 14Cfrom atmospheric

found that L. muellerii contained a record o et al. (2000b) used isotopic observations to

Mg/Ca relative to growth bands in this sam

ence of regular growth bands make rhodoli

excellent biogenetic archive of year-to-year

environmental conditions (Halfar 1999; Hal

The growth rates of subtropical G

markedly among species with strong seaso

using field and laboratory experiments, a variation in 14C, both found that L. muelle

Paz (bed 49 in fig, 3,1) had an average api

0.6 mm/yr. Using methods similar to Ri

(pers, obs,) found a similar growth rate fo

chos (bed 21 in fig, 3,1) in the central Gulf

(2oo7a), also using vital stains in the field , f

·40 ·60 ·80 ·100 ·120 1920

1940

1960

1980

2000

Year of growth: Rhodolith

3.5. 14C record from

Lithothamnion muellerii plotted with the global ocean surface remperature atlas (GOTSA) ENSO 3 sea-surface temperature (SST) anomaly.

Three large EJ Nino events are shown (highlighted in gray) that occurred coincidentally with three large declines in the 14C record of the rhodolith. From Frantz et al. (2000).

in both L. margaritae (2.8 mm/yr) and N. trichotomum (3.9 mm/yr) at the Isla El Requeson bed (bed 27 in fig 3. I) and in N. trichotomum (4.9 mm/yr) at Manto Diguet (bed 42 in fig'. 3.I). Strong seasonal growth patterns measured in L. margaritae at Isla El Requeson (5.0 mm/yr in summer vs.

0.83 mm/yr in winter; Steller et al. 2oo7a) and in L. muelleri at La Paz

(0 .2 mm/yr in summer vs. 0.5 mm/yr in winter; Rivera et al. 2004) suggest the need for further studies to understand seasonal growth trends.

Overall these slow growth rates strongly suggest that recovery of rhodolith populations from both natural and anthropogenic disturbances will be slow-on the order of decades for all species (Steller 2003).

The Diuersity of Rhodolith Communities It has long been recognized that rhodolith beds harbor a diverse and abundant assemblage of macro organisms and that this high diversity is

62/ RJOSMENA-RODRfGUEZ ET AL.

Tfl8lE 3.2. Comparison showing that (a) ov

much higher than surrounding sand flats, a to bed diversity (from Steller et al. 2003).

Subhabit

A. Richness Organism Type Epiflora

Surface

Epifauna Cryptofauna Infauna

Surface

Rhodolit Sedimen

Total

B. Density Organism Type Epifauna (#/m 2)

Surface

Cryptofauna (#/m 2 ) Infauna (#/m 2 to ro cm depth)

Sedimen

Rhodolit

Estimated total abundance (#/m 2)

NOle: x = subhabitat not present; S.E. = standard err number of species in the rhodolith bed is 52 ow infauna.

* Total

largely a consequence of the diverse an

vided by the hard, complex structure o

sediment (Weber-Van Bosse and Fosl

come to similar conclusions based on s (reviewed in Steller et al. zo03). Using

Concepcion (bed Z4 in fig. 3.r) with hig

et al. (zo03) found that overall rhodolit

high as that in the surrounding sand f

tion to bed diversity was from the cryp

among, and bored into the branches ofli

faunal diversity also increased as the bra

doliths increased, relationships of consi (discussed in a later section). Steller et

ties of organisms (>0.5 mm) inside rh

summer) study of primarily L. margaritae cryptofauna by Medina-Lopez

(1999) found 118 taxa in the 160 rhodoliths collected. There were about 10

taxa and 32 individuals per rhodolith, with crustaceans being most diverse

and abundant. There were surprisingly few differences between bed types or

seasons. Hinojosa-Arango and Riosmena-Rodriguez (2004) found a total of 104 cryptofaunal taxa (52 identified to species) in 120 large (4-5 cm diameter)

individual rhodoliths, 100 L. margaritae and 20 N. trichotomum with similar branch densities, collected from two sites in Bahia Concepcion and bed 33 (fig. 3.1) at Isla Coronado. As found by Medina-Lopez (1999), crustaceans

were the dominant group in all samples. Cryptofaunal diversity and abundance were similar in L. margaritae from the two sites in Bahia Concepcion,

averaging about 10 taxa and 75 individuals per rhodolith. Diversity and abundance were similar between the two rhodolith species from Isla Coronados, with the exception of higher crustacean abundance in N. trichotomum.

These studies suggest generally similar diversity and abundance among the cryptofauna in rhodolith beds in the Gulf dominated by

L. margaritaeiN. tl'ichotomum. These rhodoliths have similar morphology.

That rhodolith species with substantially different morphologies may harbor different cryptofauna has been shown by surveys at Cabo Los Machos near the mouth of Bahia Concepcion (Foster et aI. 2007). The wave bed at

this site (bed 21 in fig. 3.1) is dominated by high densities (ro-so/m 2) of

L. muellerii (fig. 3.3C) growing in patches of carbonate sediment intermixed with cobbles and boulders. The individual rhodoliths have thick

(~1

cm),

densely packed branches, so that the cryptofauna consists primarily ofboring organisms and other species that occupy spaces produced by borers.

Fifteen rhodoliths, five from each of three size classes, were collected at random within the site and then gently broken apart; from these, the cryptofauna were extracted and identified. A total of 117 taxa (107 species) were

64/

RIOSMENA-RODRIGUEZ ET AL.

found, with polychaetes the most diverse group

rhodolith (8.5-12 cm diameter) contained 37.8

ten contained mantis (Neogonodactylus .zacae M gebia rugosa Lockington) shrimp. This average

found in three large L. margaritae (table 3.2); a

all specimens combined, although from many fe

that found by Medina-Lopez (1999) and Hinoj Rodriguez (2004) . Although from different sam

data from all of these cryptofauna surveys sugge

nal diversity is high and is similar among species

Future understanding of rhodolith bed structur

and time would be facilitated by the use of sim methods, as described in Steller et al. (2007b).

The species richness of rhodolith beds the Gulf is further illustrated by the work of Cin

They found a total of 142 mollusc taxa larger tha tropods) in

I

X 0.2 m core samples taken from

the Bahia Concepcion/Punta Chivato region an

San Lorenzo (bed 48 in fig. 3.1). Moreover, in a commonly attached organisms are often found l lith beds. Reyes-Bonilla et al. (1997) found five

(coralliths) in rhodolith beds in the southweste

new distributional records. Two bryolith (free were also reported by James et al. (2006) at rhod southwestern Gulf.

Considerable taxonomic work remains

collections from rhodolith beds in the Gulf, a

reveal new species and biogeographic insights. identified eight species of small (2-10 mm) cry

primarily from L. margaritae in the southwester new to science. Clark commented that the chit

beds is "particularly rich and diverse." It is cle

particularly individual rhodoliths are "diversity California.

In addition to the rhodoliths thems

ten harbor a diversity of other macroalgae, an

deeper beds than in shallower beds, perhaps because oflower water temper

atures (to 17째C), lower variation in water temperatures, reduced surge, an

higher nutrients. Microalgal cover (diatoms and cyanobacteria) was hig

in summer. The elevated summer water temperatures (to 30째C), potentia

anoxic conditions at some sites, and thermal stratification likely influenc

the low summer algal diversity, leading to the disappearance of most folios

red algae and the dominance of more tolerant microalgae (Lechuga-Devez

et al. 2000). Similar seasonal patterns in macroalgal diversity have been de

scribed for rocky shores in the southern Gulf of California (Paul-Chave

and Riosmena-Rodriguez 2000) and in Bahia Concepcion (Mateo-Ci

et al. 1993).

The fishes associated with rhodolith beds are not well known. Ou

qualitati ve observations suggest that fish di versity, at least oflarger specie

that spend considerable time in the water column, is low. This is probabl because, at spatial scales larger than

~ 5-IO

cm, most rhodolith beds ar

largely two-dimensional, providing few structures to associate with. Re

ports of numerous larger fishes in rhodolith beds (see, e.g., Aburto-Oropez and Balart 2001) may be an artifact of the beds being in close proximity t

rocky or other reefs that provide macrostructure. We have noted numerou

gobies and blennies on, in, and among rhodoliths, and these fishes may b

quite diverse given the complex, small-scale structure of rhodolith beds This would be an excellent topic for future study. Large, bottom-dwellin

or burrowing species can be quite common, including tiger snake eel

(Myrichthys maculosus Curvier), bullseye electric rays (Diplobatis ommanat Jordan and Gilbert) and other rays, and Cortez garden eels (Taeniconge digueti Pellegrin).

The distribution of rhodolith beds appears to be largely constraine

by abiotic variables (discussed previously). However, within-bed commu

nity structure, and perhaps even bed persistence, may be strongly affecte

66/

RIOSMENA-RODRIGUEZ ET AL.

by species interactions. For example, b may, by moving rhodoliths and resusp dolith growth and bed maintenance (M produced by invertebrates may also be four new chiton species described by tat provided by living rhodolith bran abundant in rhodolith beds in the Gu Cintra-Buenrostro et al. zooz; Hall-S from larval settlement preferences for or other structured or large-grain subs cies inside rhodolith beds, and the refu (Steller Z003).

Yet these positive attributes o dilemma because of the degradation (Hall-Spencer 1998, 1999; Hall-Spen typically found in the diet of the gree Z003) and its foraging grounds (revi zooS) in Bahia Magdalena are commo rhodolith sediment (Iglesias-Prieto et habitats (Rjosmena-Rodriguez, unpub otic and abiotic factors may be especia motion patterns responsible for rhodo larval delivery of a number of associat remain to be investigated .

Sediment Production and

Foster (ZOOI) described a mo of rhodoliths, rhodolith beds, and th them. Rhodolith frag路ments can be bro bance by water motion, bioturbation, g also produce sand and smaller calcare cur from sedimentation and during/a recognized worldwide as "carbonate f and as important sources of modern c Schlanger and Johnston 1969; Halfar

material making up a fossil sand dune on Isla Coronado is rhodolith derived

They estimate that it would take 8,640 rhodoliths 5 cm in diameter to mak 1 m 3 of material. Johnson and Hayes (1993) described rhodolith beds as on of the most common elements in Pleistocene deposits. Like living beds i

modern nearshore areas, fossil rhodolith deposits are often the dominan elements in Pleistocene deposits in the Loreto area (Dorsey 1997), Bahi

Concepcion (Meldahl et al. 1997), and Punta Chivato (Simian and Johnso 1997)' Qlantitative methods used by Russell and Johnson (2000) and d Diego-Forbis et al. (2004) revealed a mixture of molluscs and corals wit rhodoliths in fossil records from the Gulf. Studies in the Gulf have use fossil rhodoliths to delimit coastal areas near paleo-islands and other paleo

ecological settings (Johnson and Ledesma-Vazquez 2001) .

Forrest et al. (2005) found that rhodolith beds are involved in de termining the geochemistry of hydrothermal gas samples from the El Re queson Fault Zone in Bahia Concepcion, suggesting that the thermal de composition of organic and carbonate-rich sediments is a significant sourc of the N z, CO, and CH 4 in the gas. The d i3 C values of the CH 4 were con sistent with deri vation of the gas by thermal cracking of marine algal kero

gens, or pseudo kerogens; and the d I3 C values of the COz indicate that th dissolution of rhodolith calcium carbonates may contribute to the levels o CO 2 in the gas .

.flnthropogenic Disturbance and Conseruation

As previously discussed, water motion maintains rhodolith popu lations in a gTowing, unattached, and unburied state, and it also influence thallus complexity. However, extreme water motion can result in the de struction of plants. The primary persistent natural disturbances in rhodo

68/ RIOSMENA-RODRIGUEZ

ET AL.

THBlE 3.3. Species found

beds that are protected un Mexican Directive for Spe Some Threat" (NOM-EC Taxonomic Group

Sp

Cnidaria

Psa Po Po Fu Fu lso Pil Spo

Holothuroidea Bivalvia

lith beds are water motion and sedimentat

ter 2001), bioturbation (Marrack 1999; Ja

changes in temperature and nutrient regim

tors including decreased water quality, ext

Grave and Whitaker 1999; Hall-Spencer a

ute to the burial and destruction of thalli

pendent upon some degree of disturbance

els of disturbance can result in reduced th

loss of living thalli; and ultimately a transi

carbonate sand flats. The greatest loss in predicted to be in cryptofaunal organisms

substrate not found in soft sediments (Ste

In the Gulf of California, commer

using hookah to harvest scallops and other

servations in rhodolith beds in Bahia Conc

almost complete extraction of adult scallo

rhodolith beds caused by boat anchors, dra

tom, and direct diver disturbance while ha

obs.) . Large areas of broken rhodolith frag

rhodoliths were common in previously in

cover) where fishing operations had take

Gu\t ot Ca\iJornia rhodolith beds has be

Gastropoda

Bivalvia

SterlOplax mariposa Retusa xystrum Hexapfex ( = Muricanthus) nigritus iVlegapitaria squalida Argopaten verltricosus ( = A. "ircu faris) Lyropecten subnodosus Pinna rugosa Modiolus capax

(Hall I992), but its extent and severity is unknown. It is clear that traw ing for bivalves in rhodolith beds reduces epifauna and in faunal divers through large-scale homogenizing of the benthos (Hall-Spencer I999).

It is not only the direct removal of thalli but also the alteration

their morphology that can affect species diversity and abundance. Thu

even disturbances with relatively low impacts may have severe effects at t

community level. Whereas the direct impact of species harvest and the lo of habitat structure on species abundance can be measured, indirect effe

are more difficult to estimate. For example, the direct effects of trawli

or bottom fishing for scallops and other benthic species include decreas

abundance of the target species, but it also indirectly influences comm

nity structure by decreasing fragile or omnivorous species, increasing sp

cies that feed on soft-sediment suspension (Grall and Glemarec I997), a increasing the number of scavengers (Hall-Spencer and Moore

2000

Long-term effects are difficult to estimate, bur it is clear from extreme

low coralline growth rates-both worldwide and in the Gulf-that reco

ery of the substrate after disturbance is likely to be very slow. Findings fro

the Gulf of California demonstrate that (I) rhodolith beds are important

maintaining the diversity and abundance of benthic species, including ec

nomically important species; and (2) as also found by Grall and Glemar

70 I

RIOSMENA-RODRIGUEZ ET AL.

THBlE 3.5. Comparative analysis of the cons habitat and rhodolith-forming species.

UK'

European Union'

Rhodohth lmaerl beds as habitat Protected und er the Special Areas of Conservation (SACs) in England , Scotland, and Northern Ireland

Legally protected by the European Community Council Directive'

Species protected Phymatolithon calcareum P cakareum & L. coral/ioides (Pallas) Adey & McKibbin, LithothamnioJt coral/ioides Crouan & Crouan; Lithothamnioll glaciale Kjellman has been proposed for listing on EC Habitats Directive

'Council Directive 92 /43 /EEC (1992); protected under bDirector of National Parks (ZOOS). ' Department of Conservation (1998).

(1997), maintenance of high cover of in imperative to maintaining high diversity.

As a consequence of our long-ter liths, we have been able to identify at lea

ily in rhodolith communities (table 3.3) to protect species (Dial'io Oficial 2002a) of special consideration because at least

(table 3-4) are usually found in this enviro dolith beds and rhodolith-forming specie tion in several parts of the world (table 3 of Conservation in Europe and the Unit

ered in the development of marine parks designing marine reserves in the Gulf, Sa as one of the relevant habitats for conserv protected areas (Loreto, Isla Espiritu S

and R. Brusca for his encouragement, help, and patience. The research upon which this review is based would not have been possible without the support of BCSES, CONABIO, CONACYT, USA/Mexico Fulbright Program, Inter American Institute for Global Change Research, Moss Landing Marine Laboratories, UC Santa Cruz, National Geographic Society, Packard Foundation, and UCMEXUS over the last 15 years. We also thank

J. Ruprow, C. Sanchez, E. Ochoa, and O. Aburto for their ongoing interest in rhodolith beds and reports of many new locations.

P. Raimondi,

at least 750 years in studying the Gulf of California. and the chapters document both excellent science and serious environmental degradation .

This book will be an instant classic."

-

raul Dayton. Scripps Institute of Oceanograp~

"Richard Brusca. as editor and contributor. has assembled a team of research scientists with long-time experience investigating the Sea of Cortez. Coliective~l. they have thorough!;, reviewed the status of knowledge of this sea. presenting a baseline for ecological monitoring as commercial exploitation and global climate change challenge the ecosystems of the Gulf of California."

-

Donald A. Thomson. Professor Emeritus. Universi~ of Arizona

ISBN 978路0路8165路2739路7

I

780816 527397