Territorial damselfish enhances multi-species co-existence of foraminifera mediated by biotic habitat structuring

The structures of benthic foraminiferal communities inside and outside the territory of the pomacentrid damselfish Stegastes nigricans on coral rocks in a moat of Sesoko Is. (26°38′N, 127°52′E) in Okinawa, Japan were compared. Inside the territory, an algal farm, i.e., a dense stand of a filamentous rhodophyte, Womersleyella setacea, was maintained throughout the year. Outside the territory, in areas subjected to intensive and continuous grazing by various grazers, the flora was composed of mat-like cyanophytes, a prostrate turf-form Padina sp., microscopically thin filaments and scattered filamentous rhodophytes. Algal biomass was greater inside the territory than outside the territory of the damselfish. These differences were reflected by the structure of the associated foraminiferal communities. We classified foraminiferal species based on their microhabitat use around algal communities into four life types: free-living type, crawling type, sedentary type, and sessile type. The abundance of foraminifera, especially the free-living type (e.g., Peneroplis pertusus and Quinqueloculina seminulum) and sedentary type (Rosalina globularis and Cymbaloporetta squammosa), was greater inside the territory of the damselfish than outside the territory. Species richness was also higher inside the territory, mainly due to an increase in species richness of the free-living and sedentary types. These increases in abundance and species richness were caused by habitat structuring. W. setacea is a relatively tall and complicated alga with tangled rhizoids. Its dense stand inside the territory trapped a larger amount of sediment, which provided free-living foraminifera with heterogeneous and stable habitats. In addition, the dense stand of W. setacea provided sedentary-type foraminifera with a large, complex substratum, providing refuge and food inside the territory. This assumption was confirmed by the results of plate experiments showing that foraminiferal community structures were controlled by associations between foraminifera and algae. We showed that habitat-conditioning is an important process in biotic habitat-structuring and that habitat-conditioning by territorial damselfish maintains and enhances multi-species coexistence of foraminifera on coral rocks in a coral reef.     

Territorial behavior of threespot damselfish (Eupomacentrus planifrons) increases reef algal biomass and productivity

Synopsis Algal growth and damselfish (Eupomacentrus planifrons) territories were studied in two reef habitats at Discovery Bay, Jamaica. Damselfish territories were contiguous in the reef flat (0 to 2.5 m), where the algal composition and biomass varied from territory to territory. In contrast, on the lower reef terrace (22 m), damselfish territories were often spatially segregated. While the algal composition of the territories was more uniform on the reef terrace, the total algal biomass was lower than in the territories on the reef flat. Damselfish are largely herbivorous, and they defend their territories against most intruding fish, including a number of herbivorous species. Areas of the reef terrace outside of damselfish territories were heavily grazed by herbivorous fishes and contained only small quantities of non-crustose algae.The reef terrace territories were characterized by a multispecific turf of algae (greens, blue-greens, and reds) covering the Acropora cervicornis framework and by the leafy, brown alga, Lobophora variegata. A rapid reduction in the biomass of brown algae and filamentous algae was noted when damselfish were permanently removed from their territories. Only calcified, encrusting algae — plants apparently somewhat undesirable as fish food sources — would be common on the terrace zone of this reef if damselfish territories were absent. Damselfish territoriality may significantly influence the dynamics of some reefs by increasing the biomass of the algal turf thereby increasing; reef productivity. Since blue-green algae, potential nitrogen fixers, occur in these algal turfs, the fish may also be indirectly affecting reef nutrition.     

Food habits of the farmer damselfish <Emphasis Type="Italic">Stegastes nigricans</Emphasis> inferred by stomach content,stable isotope,and fatty acid composition analyses

The territorial damselfish, Stegastes nigricans, maintains algal farms by excluding invading herbivores and weeding unpalatable algae from its territories. In Okinawa, Japan, S. nigricans farms are exclusively dominated by Polysiphonia sp., a highly digestible filamentous rhodophyte. This study was aimed at determining the diet of S. nigricans in Okinawa and its dependency on these almost-monoculture algal farms based on stomach content and chemical analyses. Stomach content analyses revealed that all available food items in the algal farms (i.e., algae, benthic animal inhabitants, trapped detritus) were contained in fish stomachs, but amorphous organic matter accounted for 68% of the contents. Therefore, carbon and nitrogen stable isotope ratios and fatty acid (FA) compositions were analyzed to trace items actually assimilated in their bodies. Stable isotope analyses showed that benthic animals were an important food source even for this farmer fish. Two essential fatty acids (EFAs), 20:4n6 and 20:5n3, which are produced only by rhodophytes among available food items, were rich in the muscle tissue of S. nigricans as well as in algal mats and detritus, suggesting that algal mats contribute EFAs to S. nigricans directly and indirectly through the food web. In conclusion, S. nigricans ingested algal mats, detritus, and benthic animals maintained within its farm. Algae and detritus were original sources of EFAs, and benthic animals, which were much more abundant in the farms than in outside territories, provided a nitrogen-rich dietary source for the fish.     

Modification of benthic communities by territorial damselfish: a multi-species comparison

The effects of territorial damselfish on coral reef benthos have been well-studied for a few relatively large-bodied species with visually distinct territories. Despite a growing body of research demonstrating their abundance, and their effects on algae, corals and other grazers, there has been little research on the effects of the territorial damselfish community as a whole. This study investigated the space occupation, territory composition, and diet of ten damselfish species at three locations: Magnetic and Orpheus Islands (Great Barrier Reef), and Kimbe Bay (Papua New Guinea). Territories were measured, and the composition of benthic communities inside and outside territories was assessed both in situ and from algal collections. The stomach contents of territorial damselfishes were also quantified. Although the larger, previously well-studied species had the most visible effect on the benthic community in their territories, all the smaller species also significantly affected the algal composition, normally with an increase of palatable algae. However, the composition of algal assemblages inside the territories of different species varied considerably. Damselfish territories were highly individual, not just among species, but also among locations. Diets were diverse and indicated a greater degree of omnivory and detritivory than previously thought. At all locations, territories occupied a substantial proportion of the substratum: >25% on Magnetic Island, >50% at Orpheus Island, and ∼50% in Kimbe Bay. Within individual zones, this figure was as high as 70%. The contribution of territorial damselfishes to a range of benthic patterns and processes is considerable, and future benthic studies may need to distinguish more closely between territory and non-territory areas. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Interactions between herbivorous fish guilds and their influence on algal succession on a coastal coral reef

Herbivory is an important mechanism affecting algal succession, particularly on coral reefs where the relationship between algae and corals is largely controlled by herbivores. However, different functional groups of herbivores may have contrasting effects on succession, which may explain different trajectories of coral reef recovery after disturbance. Here, the effects of different herbivore groups (roving herbivores = foragers and territorial damselfish = farmers) were isolated by a multi-factorial experiment carried out on a coastal coral reef with high macroalgal cover, high farmer densities and relatively low forager abundance. The effects of foragers and farmers were distinguished by monitoring algal succession on settlement tiles placed inside and outside exclusion cages, with orthogonal treatments established inside and outside damselfish territories (with appropriate cage controls). Within 12 months, algal assemblages on ungrazed tiles inside exclusion cages proceeded rapidly from fine filamentous turfs, to corticated algae, to tough erect (e.g. Amphiroa spp.) and foliose (e.g. Peyssonnellidae) calcified algae. Farmers had a dramatic impact on succession, essentially arresting the development of the algal community at a point where it was dominated by palatable filamentous algae of the genus Polysiphonia. Fleshy macroalgae such as Sargassum spp. were excluded from farmer territories. In contrast, foragers did not suppress fleshy macroalgae, but rather, appeared to decelerate succession and promote a relatively diverse assemblage. In contrast to forager-dominated reefs, farmer territories did not appear to function solely as forager exclusion areas or promote algal diversity as a result of intermediate grazing pressure. The relatively strong effects of farmers observed here may represent a future scenario for coral reefs that are increasingly subject to overfishing of large grazing fishes.     

Effects of territorial damselfish on cryptic bioeroding organisms on dead Acropora formosa

Many damselfishes exclude other grazers from their territories and “farm” filamentous algae within their territories. In this study the indirect effect of damselfish territories on faunal composition and abundance of internal bioeroders of dead Acropora formosa (Dana, 1846) was investigated in territories of two damselfish species, Stegastes nigricans (Lacepède, 1802) and Plectroglyphidodon lacrymatus (Quoy and Gaimard, 1825). S. nigricans tends to be more protective and defend their territories more aggressively than P. lacrymatus. Newly killed branches of A. formosa were placed inside and outside damselfish territories, for 1 or 2 years, at a coral reef near Zanzibar, Tanzania. As predicted, the coral branches became covered with more filamentous algae in the S. nigricans territories than in the controls, with intermediate levels in the P. lacrymatus territories. Among the internal bioeroding fauna, polychaetes were by far the most common group. In total, there were significantly more borers in the first year than the second, which was mainly due to a high abundance of sabellids. Furthermore, sabellids were significantly more abundant in control areas and in the P. lacrymatus territories compared to the S. nigricans territories. However, many other genera showed the opposite pattern, with more polychaetes in the fish territories compared to the controls. There was also a clear difference in assemblage structure between S. nigricans territories and controls. Thus, we found strong effects of whether a piece of coral was placed inside or outside a damselfish territory on the abundance of many of the bioeroding taxa. We discuss multiple reasons for these indirect effects of the territories, including that deposit feeding bioeroders may benefit from the dense algal turf found inside the territories whereas suspension feeding bioeroders may benefit from substrate with less filamentous algae found outside territories. Considering our results in the context of the large areas of coral reefs that typically are defended as territories by damselfishes, these fish are likely to have a considerable impact on the boring community of a coral reef.     

Geographic variation in the damselfish-red alga cultivation mutualism in the Indo-West Pacific

Background  

On coral reefs, damselfish defend their territories from invading herbivores and maintain algal turfs, from which they harvest filamentous algae. In southern Japan, intensive weeding of indigestible algae by Stegastes nigricans results in overgrowth by one filamentous alga, Polysiphonia sp. 1. Because this alga is highly susceptible to grazing and is competitively inferior to other algae, it survives only within the protective territories of this fish species, suggesting an obligate mutualism between damselfish and their cultivated alga. The wide distribution of damselfish species through the Indo-Central Pacific raises the question of whether this species-specific mutualism is maintained throughout the geographic range of the fish. To address this question, from all 18 damselfish species we conducted comprehensive surveys of algal flora within their territories throughout the Indo-West Pacific, and identified species of Polysiphonia using morphological examination and gene sequencing data.     

A novel obligate cultivation mutualism between damselfish and Polysiphonia algae

In cultivation mutualisms, farming animals prepare fields for cultivars, enhance their growth and harvest them. For example, in terrestrial ecosystems, plant-herbivore cultivation mutualisms arose between humans and their crops only relatively recently. We discovered an obligate cultivation mutualism between a damselfish and an alga in a coral reef ecosystem. The damselfish, Stegastes nigricans, manages algal farms through territorial defence against the invading grazers and through weeding of unpalatable algae. As a result, the algal farms of S. nigricans are dominated by one species, Polysiphonia sp. We performed an exhaustive survey of algal assemblages inside and outside the territories of five damselfish species around the Ryukyu Islands, Japan, using molecular and morphological characteristics. Polysiphonia sp. 1 grew exclusively inside the farms of S. nigricans, and never elsewhere. Since only Polysiphonia sp. 1 is harvested and consumed by the damselfish as a staple food, this interdependent relationship is an obligate cultivation mutualism. This is the first record of an obligate plant-herbivore cultivation mutualism in a marine ecosystem. Our data also suggest that three other Polysiphonia species are facultatively mutual with, commensal with, or parasitic on other damselfish species.     

Farming behaviour of reef fishes increases the prevalence of coral disease associated microbes and black band disease

Microbial community structure on coral reefs is strongly influenced by coral–algae interactions; however, the extent to which this influence is mediated by fishes is unknown. By excluding fleshy macroalgae, cultivating palatable filamentous algae and engaging in frequent aggression to protect resources, territorial damselfish (f. Pomacentridae), such as Stegastes, mediate macro-benthic dynamics on coral reefs and may significantly influence microbial communities. To elucidate how Stegastes apicalis and Stegastes nigricans may alter benthic microbial assemblages and coral health, we determined the benthic community composition (epilithic algal matrix and prokaryotes) and coral disease prevalence inside and outside of damselfish territories in the Great Barrier Reef, Australia. 16S rDNA sequencing revealed distinct bacterial communities associated with turf algae and a two to three times greater relative abundance of phylotypes with high sequence similarity to potential coral pathogens inside Stegastes''s territories. These potentially pathogenic phylotypes (totalling 30.04% of the community) were found to have high sequence similarity to those amplified from black band disease (BBD) and disease affected corals worldwide. Disease surveys further revealed a significantly higher occurrence of BBD inside S. nigricans''s territories. These findings demonstrate the first link between fish behaviour, reservoirs of potential coral disease pathogens and the prevalence of coral disease.     

Comparative feeding ecology of two herbivorous damselfishes (Pomacentridae: Teleostei) from the Gulf of California,Mexico

Two species of benthic damselfishes from the Gulf of California, Mexico, use contrasting behaviors when feeding on benthic algal communities. The small (±70 g) Cortez damselfish, Eupomacentrus rectifraenum (Gill, 1862), feeds selectively from a multi-species algal mat, eats fleshy red and green algae and ignores brown and calcareous algae. The giant blue damselfish, Microspathodon dorsalis (Gill, 1862), is a large (±450 g), lethargic, nonselective feeder which grazes on a near monoculture of a fleshy red alga, Polysiphonia sp. Feeding activity for both species is low in the morning peaks during late afternoon, and drops sharply as night approaches. Based on feeding rates, gut-filling times, and weights of gut contents, Cortez damselfish process six to eight full guts of food and giant blue damselfish three full guts of food per day. The algal mat exhibits high standing crops (291–618 g dry wt · m^?2) and low productivity, but the preferred food of the Cortez damselfish (Ulva) appears to colonize the mat frequently and grow rapidly. The Polysiphonia dominated community on giant blue damselfish territories exhibits low standing crops (23 g · m^?2) and high productivity (34–47 times that of the mat per gram algae). Even though the feeding behaviors and resources used by the two damselfishes differ, both species eat similar food (delicate red and green fleshy algae, and depend on rapid colonization and/or high productivity to maintain their primary foods in the grazed algal community.     

Effects of the Caribbean threespot damselfish,Stegastes Planifrons (Cuvier), on algal lawn composition

Algal lawn communities within territories of herbivorous threespot damselfish, Stegastes planifrons (Cuvier) were studied in a shallow back-reef environment at La Parguera, Puerto Rico. Caging exclusion experiments, monitoring of non-manipulated lawns and gut content analyses were used to determine the effect of S. planifrons on algal species composition of the lawn. An average of 40 algal species per sampling period were found in naturally occuring lawns, with a total of 53 species being recorded throughout the course of study. Examination of algal species found in damselfish guts and comparison with natural lawns indicate that damselfish feed primarily on their algal lawns and graze the algae present in proportion to abundance. Caged algal lawns showed significant decline in algal species number and abundance over time. Non-selective feeding by Stegastes planifrons within their territorial lawns appears to result in an “intermediate disturbance” which maintains a greater algal species richness than is found in their absence.     

Experimental analysis of resource sharing between herbivorous damselfish and blennies on the Great Barrier Reef

Competition theory suggests that species with very similar resource requirements should not be able to coexist when resources are limiting. However, on coral reefs, territorial herbivorous fishes which use apparently very similar resources often coexist without competitive exclusion. This study investigates patterns of resource use by damselfish Pomacentrus flavicauda Whitley and blennies, primarily Salarias fasciatus Bloch, living in rubble habitats on the Great Barrier Reef. These species feed mainly on turf algae and have overlapping territories and home ranges. I ask two questions:

• 1.(1) is there any evidence of resource partitioning between these species; and
• 2.(2) do they compete for food or space? It is highly unlikely that damselfish and blenny species partition food resources by eating different species of algae, since species are intermixed at a very small scale in the algal turf. Instead, differences in food use were looked for by counting the numbers of bites fish of each species took from different parts of the rubble habitat.

Little difference in food use was found between Pomacentrus flavicauda and Salarias fasciatus except that the former fed on plankton to some extent whilst the latter did not. A manipulation experiment was performed to assess whether blennies inhabiting damselfish territories competed with damselfish for algae. Damselfish territories were used as experimental units and two manipulations performed:

• 1.(1) S. fasciatus removal, and
• 2.(2)Pomacentrus flavicauda removal.

There were four replicates of each with four undisturbed controls. Territory sizes, feeding rates and attack rates on other fishes of P. flavicauda were measured before and after blenny removal. Blenny density and biomass were measured before and after P. flavicauda removal. None of these measures provided evidence of exploitation competition between these species or of changes in levels of interference competition by damselfish after blenny removal. Blenny densities and biomass did not change significantly after damselfish removal. Damselfish appear to tolerate blennies within their territories because they cannot economically exclude them. However, the intermittent availability of an alternative source of algae outside damselfish and blenny territories and home ranges may mean that algae are not normally a limiting resource.     

Effects of territorial damselfish on an algal-dominated coastal coral reef

Territorial damselfish are important herbivores on coral reefs because they can occupy a large proportion of the substratum and modify the benthic community to promote the cover of food algae. However, on coastal coral reefs damselfish occupy habitats that are often dominated by unpalatable macroalgae. The aim of this study was to examine whether damselfish can maintain distinctive algal assemblages on a coastal reef that is seasonally dominated by Sargassum (Magnetic Island, Great Barrier Reef). Here, three abundant species (Pomacentrus tripunctatus, P. wardi and Stegastes apicalis) occupied up to 60% of the reef substrata. All three species promoted the abundance of food algae in their territories. The magnitudes of the effects varied among reef zones, but patterns were relatively stable over time. Damselfish appear to readily co-exist with large unpalatable macroalgae as they can use it as a substratum for promoting the growth of palatable epiphytes. Damselfish territories represent patches of increased epiphyte load on macroalgae, decreased sediment cover, and enhanced cover of palatable algal turf.     

铜锈环棱螺对水华中常见藻类的抑制效应

藻类水华频发已成为全球性的水环境问题,近年来,生物控藻法因具有环境友好的特点而备受关注。本研究以我国富营养化湖泊中常见大型底栖动物铜锈环棱螺为操纵生物,通过室内培养试验,研究了其对水华水体中常见蓝藻铜绿微囊藻、绿藻普通小球藻和斜生栅藻生长及光合活性的影响,以期阐明螺-藻间相互作用关系,探究铜锈环棱螺作为生物操纵物种的可行性。结果表明: 铜锈环棱螺能在短时间内大量摄食藻细胞,其对铜绿微囊藻产毒株和不产毒株以及斜生栅藻的去除率均在12 h内达到最大值,分别为73.7%、73.2%和51.1%;其对普通小球藻的摄食强于其他藻类,至试验结束时去除率达到99.2%。产毒铜绿微囊藻产生的微囊藻毒素会在铜锈环棱螺体内累积并促发其肝脏病理学变化,进而阻碍铜锈环棱螺的摄食。试验后期各处理组藻细胞光合活性均显著低于对照组,表明铜锈环棱螺的摄食作用对藻细胞造成了损伤,抑制了其大量增殖。此外,当不产毒铜绿微囊藻与斜生栅藻混合时,铜锈环棱螺的选择摄食性导致微囊藻的优势地位被斜生栅藻所取代。因此,铜锈环棱螺可以通过摄食作用抑制藻类的光合活性并降低其生物量,从而在一定程度上抑制或减缓水华的形成。     

As you weed,so shall you reap: on the origin of algaculture in damselfish

Within their territories, damselfish cultivate particular algae for consumption. A recent study in BMC Evolutionary Biology shows extensive variation among and within fish species in the composition of these algal 'gardens', varying from monocultures to cultures of mixed species, and in the mode of cultivation. This fish-algal agriculture may provide insight into the early stages of domestication.     

Algal assemblages associated with Stegastes sp. territories on Indo-Pacific coral reefs: Characterization of diversity and controls on growth

Herbivorous fish occupy an important niche in coral reef ecosystems. Specifically, damselfish of the genus Stegastes have been shown to have a significant impact on coral community structure and algal assemblages. This study investigated the algal communities associated with Stegastes territories of the Indo-Pacific (Fiji, Solomon Islands, and Tonga), while concurrently examining the effects of nutrient enrichment and herbivore exclusion (alone and in unison) on these communities. Results evidenced differences in species composition, percent cover, and algal growth rate between Stegastes territories and non-Stegastes sites and between control sites and treatment sites. Stegastes territories consistently displayed a greater abundance of turf algae than non-Stegastes sites; the two main genera of turf algae observed at all sites were Polysiphonia and Ceramium. Although non-Stegastes sites in Fiji, the Solomon Islands, and Tonga showed a greater percent coverage of macroalgae, they contained fewer algal species compared to Stegastes territories. In Fiji, red macroalgae decreased in the herbivore exclusion treatments, while brown macroalgae increased significantly in the herbivore exclusion and nutrient treatments. The combined effect of the herbivore exclusion and nutrient treatment at this location yielded a significantly increased turf algae growth rate compared to control sites. Growth rates of turf algae in the Solomon Islands and Tonga increased significantly in caged treatments, suggesting that damselfish of the genus Stegastes can play an important role in maintaining cropped algal beds. In summation, the results demonstrated that Stegastes sustains distinct algal assemblages which may be disrupted by reduced grazing and/or eutrophication.     

杭州湾内外海域秋季浮游动物群落的比较

本文比较了杭州湾湾外海域(122.10°-122.58° E, 30.54°-30.93° N)和湾内不同海域(北岸东侧: 121.67°- 121.87° E, 30.68°-30.83° N; 南岸东侧: 121.60°-121.85° E, 29.95°-30.24° N; 北岸西侧: 121.31°-121.56° E, 30.58°- 30.77° N)秋季浮游动物的群落组成、累积优势度曲线以及多样性指数(H')等群落结构特征, 并进行了差异性分析。结果表明: 湾外海域的群落组成与湾内海域的3个群落之间均有较大的差异。湾外海域的群落I是以中华假磷虾(Pseudeuphausia sinica)等近海种、背针胸刺水蚤(Centropages dorsispinatus)等沿岸低盐种为主, 其次是外海种。湾内南岸东侧海域的群落II主要以左突唇角水蚤(Labidocera sinilobata)等沿岸低盐种为主, 近海种次之。湾内北岸东侧海域的群落III是以真刺唇角水蚤(Labidocera euchaeta)等沿岸低盐种、虫肢歪水蚤(Tortanus vermiculus)等河口半咸水种组成的混合群落。湾内北岸西侧海域群落IV是以虫肢歪水蚤为代表的河口半咸水种为主的群落。总的说来, 这一水域向西和向北方向出现更低盐度适应性的群落。从累积优势度曲线来看, 湾外海域群落I与湾内北岸东侧群落III的累积优势度上升趋势均相对平缓, 但群落III的初始累积优势度略高于群落I; 而与群落I相比, 湾内南岸东侧的群落II与北岸西侧的群落IV的初始累积优势度均很高。湾外海域群落I的初始累积优势度较低, 显示出群落I的优势种较多, 而单一优势种优势度低于湾内3个群落。方差分析结果表明: 湾外海域的浮游动物多样性指数与湾内3个海域均有极显著差异(P < 0.01), 而湾内各海域之间均无显著性差异(P > 0.05)。说明湾外浮游动物群落的多样性高于湾内海域。湾内外海域浮游动物群落特征之间有较大差异, 其主要原因是影响各自群落的主导水团明显不同。     

低温驯化和外源糖对爪哇伪枝藻冷胁迫的影响

低温是影响荒漠藻类生存的重要环境因子.研究了低温驯化和外源糖对爪哇伪枝藻冷胁迫的作用.实验测定了低温和外源糖处理下伪枝藻某些生理活性指标的变化.结果表明,低温胁迫导致伪枝藻生物量和光合活性的显著降低,低温驯化和外源糖在一定程度上对藻细胞叶绿素α含量和光合活性具有促进作用,低温驯化明显提高了细胞内可溶性蛋白的含量,而对丙二醛的含量影响不大.研究还发现,低温驯化明显降低了细胞膜的相对透性,而外源糖对细胞膜的相对透性影响不大.此外,低温驯化促进了伪枝藻胞外多糖的大量合成.研究结果初步证实了低温驯化和外源糖类对于提高伪枝藻的冷胁迫耐受性具有调节作用.     

Effects of quantitative and qualitative variation in phenolic compounds on feeding in three species of marine invertebrate herbivores

The deterrent effects of brown algal phenolic compounds and the terrestrial polyphenolic tannic acid on feeding by three species of invertebrate herbivores from central California, including the gastropods Tegula funebralis (Adams) and Tegula brunnea (Phillipi) and the echinoid Strongylocentrotus purpuratus (Stimpson) were examined. Algal phenolics used were the monomeric phenolic phloroglucinol and polyphloroglucinols from Fucus vesiculosus (Linnaeus), Halidrys siliquosa (Linnaeus) Lyngbye and Eisenia arborea Areschoug. All of the polyphenolics deterred feeding by all three herbivores at concentrations of 5 mg · ml⁻¹ in agar disks. Concentrations of 2 mg · ml⁻¹ also generally deterred feeding by the gastropods (these levels were not tested against S. purpuratus). Relative amounts of deterrence by different compounds were similar, especially for the gastropods. Phloroglucinol deterred feeding by the echinoids, but not by T. funebralis. Responses of the echinoids were otherwise similar to the gastropods, but more variable. I also demonstrated deterrence of S. purpuratus by tannic acid using the “tanned” kelp technique of Steinberg (1985). Reactivity of the different phenolic compounds in the Folin-Denis procedure, a common colorimetric assay used to estimate levels of phenolics in plant tissue, was similar. This suggests that measuring phenolic levels in brown algae by this technique will not be greatly confounded by the occurrence of different kinds of phenolic molecules in different brown algae. This result, in combination with the similarity of the deterrent effects of the compounds used in this study, increases the validity of previous studies in the northeastern Pacific Ocean which correlate algal phenolic levels and diets or feeding preferences of invertebrate herbivores. For plants and herbivores in this region, this assay is a reasonable measure of a biologically meaningful phenomenon — levels of phenolic deterrents in the algae.     

Dual Roles of an Algal Farming Damselfish as a Cultivator and Opportunistic Browser of an Invasive Seaweed

Herbivory is a fundamental process determining reef resilience, and while algal farming damselfishes can help shape benthic assemblages, an understanding of their contribution to areas outside of defended territories is relatively unexplored. Here, we demonstrate how the farming damselfish Stegastes marginatus plays a dual role in benthic structuring by 1) contributing to persistence of the invasive macroalga Acanthophora spicifera within a Hawaiian marine protected area, where the macroalga occurred exclusively inside Stegastes territories, and 2) behaving as an opportunistic browser of the exotic alga outside their territorial borders. Greater than 50% of the biomass of tethered A. spicifera was consumed within one-hour when placed outside Stegastes territories, compared to <5% lost from tethers within territories or herbivore exclusion cages. In situ remote video revealed that tethered A. spicifera located outside territories was grazed primarily by the surgeonfish Acanthurus nigrofuscus (∼68% of total bites) and, surprisingly, by S. marginatus (∼27% of total bites) that left their territories to feed on this resource on 107 occasions during 400 min of filming. Further, for over half of those occurrences where S. marginatus grazed on the tethered macroalga outside of territories, they fed alongside conspecifics and other species, displaying little of the aggressiveness that characterizes this damselfish. These results show that S. marginatus plays a wider role in determining benthic assemblages than previously recognized, acting both as cultivators of a canopy-forming invasive macroalga within their territories, and as opportunistic browsers in neighboring sites. Consequently, S. marginatus can affect benthic species composition across their territory borders. These results provide a rare example of interspecific facilitation of an exotic alga by an indigenous marine fish. Accounting for fish behaviors more broadly is important to further our understanding of ecological processes that shape reef ecosystems to improve management of MPAs that often support extensive farming damselfish populations.