Fifty million years of herbivory on coral reefs: fossils,fish and functional innovations

The evolution of ecological processes on coral reefs was examined based on Eocene fossil fishes from Monte Bolca, Italy and extant species from the Great Barrier Reef, Australia. Using ecologically relevant morphological metrics, we investigated the evolution of herbivory in surgeonfishes (Acanthuridae) and rabbitfishes (Siganidae). Eocene and Recent surgeonfishes showed remarkable similarities, with grazers, browsers and even specialized, long-snouted forms having Eocene analogues. These long-snouted Eocene species were probably pair-forming, crevice-feeding forms like their Recent counterparts. Although Eocene surgeonfishes likely played a critical role as herbivores during the origins of modern coral reefs, they lacked the novel morphologies seen in modern Acanthurus and Siganus (including eyes positioned high above their low-set mouths). Today, these forms dominate coral reefs in both abundance and species richness and are associated with feeding on shallow, exposed algal turfs. The radiation of these new forms, and their expansion into new habitats in the Oligocene–Miocene, reflects the second phase in the development of fish herbivory on coral reefs that is closely associated with the exploitation of highly productive short algal turfs.     

Pair territoriality in the longnose filefish,oxymonacanthus longirostris

The longnose filefish,Oxymonacanthus longirostris, usually lives in heterosexual pairs, the male and female swimming together and sharing the same territory. Pair territoriality in the species was examined in detail in relation to sexual differences in territorial defense activities. Rigorous pair territoriality was maintained only during the breeding season, although pairs used their home ranges exclusively to a certain extent, during the non-breeding season. The frequency of aggression against other conspecific pairs in the breeding season was higher than in the non-breeding season. Agonistic interactions appear to be over both mates and food resources, the strict pair territoriality in the breeding season possibly being due to mutual mate guarding. In intraspecific aggressive interactions, males usually led their partner females when attacking intruders. The feeding frequency of males was much lower than that of females in the breeding season. Mate removal experiments indicated that females could not defend their original territories solitarily and their feeding frequency decreased. Conversely, males could defend territories solitarily without a decrease in feeding frequency. These results suggest that males contribute most to the defense of the pair territory, with females benefiting from territorial pair-swimming with their partner males.     

The influence of food abundance,food dispersion and habitat structure on territory selection and size of an Afrotropical terrestrial insectivore

Most tropical insectivorous birds, unlike their temperate counterparts, hold and defend a feeding and breeding territory year-around. However, our understanding of ecological factors influencing territory selection and size in tropical insectivores is limited. Here we examine three prominent hypotheses relating food abundance, food dispersion (spatial arrangement of food items), and habitat structure to territoriality in the Usambara Thrush Turdus roehli. We first compared leaf-litter macro-invertebrate abundance and dispersion, and habitat structure between territories and random sites. We then examined the relation between these same ecological factors and territory size. Invertebrate abundance and dispersion were sparsely and evenly distributed across our study system and did not vary between territories and random sites. In contrast, habitat structure did vary between territories and random sites indicating the Usambara Thrush selects territories with open understorey and closed overstorey habitat. Invertebrate abundance and dispersion within territories of the Usambara Thrush were not associated with habitat structure. We believe the most likely explanation for the Usambara Thrush’s preference for open understorey and closed overstorey habitat relates to foraging behavior. Using information-theoretic model selection we found that invertebrate abundance was the highest-ranked predictor of territory size and was inversely related, consistent with food value theory of territoriality.     

The relative influence of prior residency and dominance on the early feeding behaviour of juvenile Atlantic salmon

In many species where social hierarchy mediates conflict over resources, dominant individuals monopolize food, shelter and reproductive opportunities. The benefits of social dominance, however, can often be offset by a prior residence advantage, whereby individuals arriving first in a new habitat obtain, and subsequently defend, the most profitable sites. We investigated the relative influence of these two factors on the acquisition of feeding territories by juvenile Atlantic salmon,Salmo salar L., by placing groups of six individuals of known dominance rank sequentially into an experimental arena with feeding sites of varying quality. Dominants had an advantage over subordinates in the percentage of time spent in a good-quality feeding site and individual feeding rate. There was also a significant time of arrival effect: those individuals that arrived first in a habitat monopolized the resource. The two effects were of approximately equal strength, so that late-arriving dominant fish had similar success as prior resident subordinates. These results indicate that both dominance and prior residence are important in the feeding behaviour of juvenile Atlantic salmon, and that the two factors can have independent and additive effects.Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Determinants of territory size in the pomacentrid reef fish,Parma victoriae

Summary Factors governing the size of territories defended by the pomacentrid reef fish, Parma victoriae, were investigated, prompted by contradictory predictions in the literature concerning the effects of food supply and competitors. Observations were carried out over the non-breeding period (March–October) on a medium density population in which territories were partially contiguous. The territory size of adult fish varied between 3 and 26 m², and was inversely correlated with local densities of conspecifics. The same range in territory size was found for both males and females, which did not differ in the time they spent on territory defence and foraging activities. No correlation existed between territory size and the abundance of algal food, body size, age or time spent on territory defence. Also, there was little variation in territory size over time, despite seasonal changes in the abundance of food algae.Experimental reduction of food supplies on isolated territories of males and females had no effect on territory size. In a higher density habitat an experiment was carried out in which population density and food abundance were simultaneously manipulated. This showed that territory size was primarily determined by intraspecific interactions, as territories exhibited considerable increases in size upon removal of neighbours. No changes in the size of defended areas resulted from either artificial increases or decreases of food levels. There were also no changes in the time spent on defence of territories, foraging time or feeding rates associated with food manipulations or territory expansion, which suggested that food was not a limited resource. This conflicted with current theories proposed to explain territory defence and expansion. It is hypothesized that intraspecific interactions constrain territory size well below the optimum in terms of the abundance of preferred food algal species.     

Possible relationships between morphology,territory quality,and skin color of American Kestrels1

ABSTRACT Carotenoid‐based coloration of skin and plumage has been found to be correlated with individual quality in many species of birds during the breeding season. However, less is known about the possible role of these signals during the nonbreeding season, particularly among nonpasserines that defend winter territories. American Kestrels (Falco sparverius) are sexually dimorphic raptors that defend winter territories and possess carotenoid‐based morphological features known to be correlated with individual quality. Much is known about winter territory use and habitat segregation by male and female kestrels, but possible relationships among morphological features, individual quality, and habitat quality have not been examined. Our objective was to examine possible relationships between morphology, territory quality, and skin color of American Kestrels. Male kestrels had brighter skin than females, and the skin color of male kestrels was positively correlated with size (wing chord and tail length) and territorial quality (hunting territories with less canopy and more grass cover). No such relationships were found for female kestrels. Skin color appears to be an honest indicator of quality for male American Kestrels and may serve both intersexual (territory acquisition) and intersexual (mate choice) functions during the breeding and nonbreeding seasons.     

Prey availability affects territory size,but not territorial display behavior,in green anole lizards

The availability of food resources can affect the size and shape of territories, as well as the behaviors used to defend territories, in a variety of animal taxa. However, individuals within a population may respond differently to variation in food availability if the benefits of territoriality vary among those individuals. For example, benefits to territoriality may differ for animals of differing sizes, because larger individuals may require greater territory size to acquire required resources, or territorial behavior may differ between the sexes if males and females defend different resources in their territories. In this study, we tested whether arthropod abundance and biomass were associated with natural variation in territory size and defense in insectivorous green anole lizards, Anolis carolinensis. Our results showed that both male and female lizards had smaller territories in a habitat with greater prey biomass than lizards in habitats with less available prey, but the rates of aggressive behaviors used to defend territories did not differ among these habitats. Further, we did not find a relationship between body size and territory size, and the sexes did not differ in their relationships between food availability and territory size or behavioral defense. Together, these results suggest that differences in food availability influenced male and female territorial strategies similarly, and that territory size may be more strongly associated with variation in food resources than social display behavior. Thus, anole investment in the behavioral defense of a territory may not vary with territory quality.     

Conspecific attraction in a grassland bird, the Baird's Sparrow

ABSTRACT.   Territorial songbirds generally use song to defend territories and attract mates, but conspecific song may also serve as a cue to attract other male songbirds to a breeding site. Although known to occur in some colonial and forest-associated species, only recently have investigators examined conspecific attraction in grassland species. We used a playback experiment to examine the possible role of conspecific attraction for males searching for potentially suitable breeding habitat in a grassland specialist, the Baird's Sparrow ( Ammodramus bairdii ). Experimental playback plots and control plots with similar landscape and vegetation characteristics were established at two sites in North Dakota. Baird's Sparrows colonized three of six experimental plots and none of six control plots. Males on experimental plots established territories adjacent to the playback stations and were sometimes observed counter-singing with the playback of conspecific songs. Vegetation characteristics were similar on all study plots, and did not explain differences in bird density on our treatment plots. Although we found that playback of conspecific songs attracted male Baird's Sparrows to previously unoccupied, potentially suitable habitat, further experiments are needed to examine the importance of conspecific attraction relative to other cues that birds may use, such as vegetation features. The conservation and management implications of conspecific attraction are not completely understood, but the presence of conspecifics should be considered as a potential cue in habitat selection by all species of birds.     

Territory quality, survival and reproductive success in southern emu-wrens Stipiturus malachurus

Multi-factor analyses of territory quality in relation to fitness components of adults are rare, especially in non-migratory species. I studied the influence of multiple attributes of territory quality (habitat type and the abundance of food and predators) on the reproductive success and survival of a threatened Australian passerine, the southern emu-wren Stipiturus malachurus . The abundance of frequently-selected prey types (lepidoptera, diptera, hemiptera and larvae) varied significantly across territories according to habitat type. Reproductive success (number of offspring fledged) was highest in territories containing a greater proportion of tall shrubland, which had the highest insect abundance of any habitat. Closed heathland and sedge/rushland also had high food abundance compared to other habitat types, but higher fledging success occurred only within closed heathland, possibly because predator density was lower in this habitat type. High snake density was associated with reduced adult survival during the breeding season and a lower probability of nest success. In sedge/rushland, any benefits of prey abundance may therefore be offset by a high density of predators. Emu-wren age and size were unrelated to breeding output of pairs, suggesting that ecological factors may swamp effects of individual quality on emu-wren fitness components. Preservation of tall shrubland and closed heathland habitats appear to be of key conservation priority for emu-wrens.     

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.     

Structure of tree vegetation may reduce costs of territory defence in Eurasian Nuthatch Sitta europaea

Capsule In pastured old oak woodland, breeding pairs of Eurasian Nuthatch selected territories with significantly higher densities of trees and cavities.

Aims To define territorial borders that exist within a nuthatch population and to compare densities of trees and cavities between used and non-used parts of their available habitat in order to determine habitat preferences.

Methods The number and location of territories was estimated by mapping the individual positions of colour-ringed birds. We measured habitat characteristics in regular sampling grid (number of trees and number of cavities per 50?×?50?m) during three successive seasons and modelled probability of occurrence of nuthatch territories in the area.

Results Breeding pairs were observed to defend territories of median size between 1.46 and 2.93?ha. These sizes correspond well to high-quality habitat territories for this species. We found that pairs tended to occupy territories with higher densities of trees and cavities. Based on generalized linear mixed-effects model estimates, we found that in pastured oak woodland habitat with density of 60 trees per ha, the estimated probability of occurrence (with 95% confidence interval) of a nuthatch territory was about 96% (83?99). For cavity density, the probability of territory occurrence was about 74% (52?89) at the level of 60 cavities per ha.

Conclusion We suggest that higher tree and cavity densities reduce territory defence costs in the species because birds may use less energy during foraging, predation avoidance and competition for a nest hole.     

Coexistence of permanently territorial cichlids of the genus Petrochromis through male-mating attack

Coexistence mechanisms of permanently territorial fishes proposed hitherto have been mainly based on interspecific competition. To test the hypothesis of the coexistence through male-mating aggression (Kohda, 1995a), spacing patterns of feeding territories of three coexisting herbivorous cichlids, Petrochromis polyodon, P. trewavasae and P. famula, were investigated in a homogeneous habitat at a shallow rocky shore in Lake Tanganyika. All three species maintained individual feeding territories that were defended against both conspecifics and congenerics and rarely overlapped either intra- or interspecifically. Territories of three species were scattered and covered almost all rocky bottoms. Territorial attacks usually occurred near the border of feeding territories. But male P. polyodon, the largest and socially most dominant fish, attacked conspecific males far beyond their feeding territories, which were widely separated. Removal of some territory owners suggested that such attacks result in the separate distribution of male P. polyodon territories. The interstitial space between P. polyodon feeding territories resulting from their mating aggression can be occupied by subordinate congeneric fishes. Male-mating attack of dominant males of Petrochromis will facilitate the coexistence of other congeners.     

Group foraging by the herbivorous cichlid fish,Petrochromis fasciolatus,in Lake Tanganyika

Group foraging of the algae eating cichlid,Petrochromis fasciolatus, was studied along a rocky shore in Lake Tanganyika, in an area occupied by the feeding territories of several herbivorous cichlid species. SolitaryP. fasciolatus or schools comprising a few members only were nearly always repelled from such territories, although larger schools (40–250 individuals) ofP. fasciolatus were able to overwhelm the defenses of territory owners and enable subsequent foraging. The frequency and duration of individual foraging sessions on the algal mats were positively correlated with group size, probably owing to individuals in large schools suffering fewer attacks from territory owners. Almost all of the foraging sites ofP. fasciolatus were inside the territories of other herbivorous cichlids, especially those ofNeolamprologus moorii (more than 80% of total), in which the algal density was more than 10 times that in territories of the other species.N. moorii territories included only 4% rocky substrate, indicating that schools ofP. fasciolatus selectively chose territories containing rich resources.     

Feeding selectivity in relation to territory size in a herbivorous reef fish

Summary Territory size in the herbivorous reef fish, Parma victoriae, (Pisces: Pomacentridae) is primarily determined by local density patterns and is independent of changes in food levels (Norman and Jones 1984). However, while individual readily expand territories in response to having their neighbours removed, they appear not to increase total food consumption. Individuals with large territories may benefit from improved food quality. Here we test the hypothesis that expanded territories increase access to preferred food types.A preliminary comparison of the relative proportions of algal species consumed and those present in the field indicated that feeding was highly selective. Strong feeding preferences were indicated by a field cafeteria experiment, in which algal species were presented to individuals in equal amounts. Selectivity indices calculated from diet and availability measures were positively correlated with the feeding preference rankings.Individuals examined from two territory size categories (<10 m² and > 10 m²) did not exhibit significant differences in feeding prefernces. However, they differed greatly in terms of the makeup of their diets. Higher ranking algae such as Champia zostricola and Rhodoglossum sp. were consumed in greater proportions on large territories. Algal abundances within territories also differed for the two groups. Some of the less abundant, high ranking food species were found in greater quantities per unit area on large territories. The differences in diet were not solely explained by changes in availability. The appropriate comparison showed that whereas individuals on large territories fed in a highly selective manner, those on small territories consumed algae in proportion to their availability. A neighbour removal experiment supported the hypothesis that territory expansion results in an increase in the consumption of preferred algal species.     

Diet disparity among sympatric herbivorous cichlids in the same ecomorphs in Lake Tanganyika: amplicon pyrosequences on algal farms and stomach contents

Background

Lake Tanganyika, an ancient lake in the Great Rift Valley, is famous for the adaptive radiation of cichlids. Five tribes of the Cichlidae family have acquired herbivory, with five ecomorphs: grazers, browsers, scrapers, biters and scoopers. Sixteen species of the herbivorous cichlids coexist on a rocky littoral slope in the lake. Seven of them individually defend feeding territories against intruding herbivores to establish algal farms. We collected epiphyton from these territories at various depths and also gathered fish specimens. Algal and cyanobacteria community structures were analysed using the amplicon-metagenomic method.

Results

Based on 454-pyrosequencing of SSU rRNA gene sequences, we identified 300 phototrophic taxa, including 197 cyanobacteria, 57 bacillariophytes, and 31 chlorophytes. Algal farms differed significantly in their composition among cichlid species, even in the same ecomorph, due in part to their habitat-depth segregation. The algal species composition of the stomach contents and algal farms of each species differed, suggesting that cichlids selectively harvest their farms. The stomach contents were highly diverse, even between species in the same tribe, in the same feeding ecomorph.

Conclusions

In this study, the amplicon-metagenomic approach revealed food niche separation based on habitat-depth segregation among coexisting herbivorous cichlids in the same ecomorphs in Lake Tanganyika.

     

The effect of territory quality on female preference in Metriaclima zebra

The cichlid fishes of Lake Malawi are an excellent model group with which to study adaptive radiation and speciation; due to the vast number of individual species, large variation in feeding adaptations and behaviours, and relatively recent divergence are found. Males of many cichlid species will obtain and defend lek‐like territories, where they court potential mates in addition to foraging for food. Aspects of territory quality warrant investigation because of the relationship between reproductive success and territory defence success. In this study, we tested whether the presence of a small or large food resource had any effect on the preference of a gravid female for a potential mate. The results of this experiment suggest that the presence of a large food resource increases the attractiveness of a male to a potential mate. This may suggest that the presence of food alone may not be the most important factor, or there may be a threshold amount over which females are attracted. These results indicate that certain aspects of territory quality such as habitat type or proximity to a food resource may play a role in both intersexual and intrasexual selection mechanisms: perhaps even driving and possibly accelerating the speciation of certain lineages of cichlid fishes.     

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.     

Conflicting Territory Use in Males and Females of a Monogamous Ungulate,the Kirk's Dikdik

In monogamous mammals it is often unclear why males do not defend larger territories to attract more than one female. I investigated the territoriality of the monogamous Kirk's dikdik, Madoqua kirki, a dwarf antelope, in which food resources increase with territory size and some males defend enough resources for more than one female. Yet, all males are paired monogamously. When males were removed from small territories, their female partners spent more time outside of their territories than females in large ones. When females were removed, their male partners almost never left. Pairs in small territories spent more time together than pairs in large ones. Paired males left mostly together with their females, apparently not on their own initiative. Presumably because females in small territories left more often, their males spent more time outside in the female's company than males in large territories. I argue that males in smaller territories can keep better track of their females and that they can effectively reduce their females' time outside. Male intrusion pressure was unrelated to territory size, but it increased in the presence of unguarded females. If large territories decrease the ability to mate guard, and if unguarded females attract competing males, then defending large territories may be uneconomical, even it they could attract more than one female. On the other hand, territories must be large enough to satisfy the requirements of a single female.     

The sympatric breeding of Larus fuscus, L. cachinnans and L. argentatus in western France

An opportunity to study the validity of the species Larus cachinnans , considered by some authors as merely a group of races related to either L. fuscus or L. argentatus , is given by its sympatric breeding with these species. Both of these latter species have recently extended their breeding range southwards, while Mediterranean representatives of the cachinnans group have spread northwards, and the three forms now breed side by side over c. 350 km along the Atlantic coast of France, where their breeding biology was studied from 1983 to 1990. L. cachinnans is very territorial, some pairs holding territories almost all year round; argentatus pairs may defend territories from mid-winter; and the supposedly migratory fuse us are on their territories for only a short period before laying. L. cachinnans is an early breeder, laying from late March to early May, while fuscus lay from May into June, and argentatus has a protracted breeding season overlapping the other two. Interbreeding occasionally occurs; it can be productive in the case of fuscus x argentatus whereas fuscus x cachinnans attempts did not produce any young. No cachinnans x argentatus pair has been observed. This indicates strong reproductive isolation, evidence that L. cachinnans must be considered a good species.     

Predation Risk,Resource Quality,and Reef Structural Complexity Shape Territoriality in a Coral Reef Herbivore

For many species securing territories is important for feeding and reproduction. Factors such as competition, habitat availability, and male characteristics can influence an individual’s ability to establish and maintain a territory. The risk of predation can have an important influence on feeding and reproduction; however, few have studied its effect on territoriality. We investigated territoriality in a haremic, polygynous species of coral reef herbivore, Sparisoma aurofrenatum (redband parrotfish), across eight reefs in the Florida Keys National Marine Sanctuary that were either protected or unprotected from fishing of piscivorous fishes. We examined how territory size and quality varied with reef protection status, competition, predation risk, and male size. We then determined how territory size and quality influenced harem size and female size to understand the effect of territoriality on reproductive potential. We found that protected reefs trended towards having more large predatory fishes and that territories there were smaller but had greater algal nutritional quality relative to unprotected reefs. Our data suggest that even though males in protected sites have smaller territories, which support fewer females, they may improve their reproductive potential by choosing nutritionally rich areas, which support larger females. Thus, reef protection appears to shape the trade-off that herbivorous fishes make between territory size and quality. Furthermore, we provide evidence that males in unprotected sites, which are generally less complex than protected sites, choose territories with higher structural complexity, suggesting the importance of this type of habitat for feeding and reproduction in S. aurofrenatum. Our work argues that the loss of corals and the resulting decline in structural complexity, as well as management efforts to protect reefs, could alter the territory dynamics and reproductive potential of important herbivorous fish species.