Positive feedbacks between bottom-up and top-down controls promote the formation and toxicity of ecosystem disruptive algal blooms: A modeling study

Harmful algal blooms that disrupt and degrade ecosystems (ecosystem disruptive algal blooms, EDABs) are occurring with greater frequency and severity with eutrophication and other adverse anthropogenic alterations of coastal systems. EDAB events have been hypothesized to be caused by positive feedback interactions involving differential growth of competing algal species, low grazing mortality rates on EDAB species, and resulting decreases in nutrient inputs from grazer-mediated nutrient cycling as the EDAB event progresses. Here we develop a stoichiometric nutrient–phytoplankton–zooplankton (NPZ) model to test a conceptual positive feedback mechanism linked to increased cell toxicity and resultant decreases in grazing mortality rates in EDAB species under nutrient limitation of growth rate. As our model EDAB alga, we chose the slow-growing, toxic dinoflagellate Karenia brevis, whose toxin levels have been shown to increase with nutrient (nitrogen) limitation of specific growth rate. This species was competed with two high-nutrient adapted, faster-growing diatoms (Thalassiosira pseudonana and Thalassiosira weissflogii) using recently published data for relationships among nutrient (ammonium) concentration, carbon normalized ammonium uptake rates, cellular nitrogen:carbon (N:C) ratios, and specific growth rate. The model results support the proposed positive feedback mechanism for EDAB formation and toxicity. In all cases the toxic bloom was preceded by one or more pre-blooms of fast-growing diatoms, which drew dissolved nutrients to low growth rate-limiting levels, and stimulated the population growth of zooplankton grazers. Low specific grazing rates on the toxic, nutrient-limited EDAB species then promoted the population growth of this species, which further decreased grazing rates, grazing-linked nutrient recycling, nutrient concentrations, and algal specific growth rates. The nutrient limitation of growth rate further increased toxin concentrations in the EDAB algae, which further decreased grazing-linked nutrient recycling rates and nutrient concentrations, and caused an even greater nutrient limitation of growth rate and even higher toxin levels in the EDAB algae. This chain of interactions represented a positive feedback that resulted in the formation of a high-biomass toxic bloom, with low, nutrient-limited specific growth rates and associated high cellular C:N and toxin:C ratios. Together the elevated C:N and toxin:C ratios in the EDAB algae resulted in very high bloom toxicity. The positive feedbacks and resulting bloom formation and toxicity were increased by long water residence times, which increased the relative importance of grazing-linked nutrient recycling to the overall supply of limiting nutrient (N).     

An investigation of non-steady-state algal growth. I. An experimental model ecosystem

In order to test rigorously the transient behaviour of mathematical models of algal growth, detailed laboratory data sets with good temporal resolution are required. A series of algal growth experiments was conducted in transient conditions. Monoculture growth of, and competition for nutrients between, three contrasting species of phytoplankton (the diatom Thalassiosira pseudonana, the harmful flagellate Heterosigma carterae and the toxic dinoflagellate Alexandrium minutum) were investigated in different temperature, light and nutrient regimes. Although growth dynamics were qualitatively similar in batch culture, quantitative differences were evident in the growth response of the different species when grown in single yield-limiting nutrient conditions in identical physical conditions. Quantities such as the carbon:nitrogen (C:N) ratio and C and N per cell varied between species and within species under different growth conditions. Such results have particular significance to the development of mathematical models, which commonly represent algal populations as a single homogeneous group using a single currency such as numbers, C or N. Changes in light and temperature regime influenced algal growth: Alexandrium failed to grow at low temperatures, while specific growth rates of Thalassiosira were more sensitive to changes in temperature than those of Heterosigma. Changes in the dominant organism(s) and/or its size or nutrient status may influence the transfer of nutrients within the food web. Commonly, mathematical models make cell growth a function of a single yield-limiting nutrient. Decreased growth rates and high residual nutrient concentrations in competition experiments indicate that this approach is unlikely to be successful in conditions of limited supply of more than one nutrient, where multiple nutrient stresses will be significant.      

Nutrient interactions between phytoplankton and bacterioplankton under different carbon dioxide regimes

Light, nutrients, temperature, pH, and salinity are important factors in controlling the growth of phytoplankton and bacterioplankton. Supply of key nutrients to these communities can result in mutualistic or competitive relationships between bacterioplankton and phytoplankton. In this study, we investigated growth and uptake of nutrients by the marine prasinophyte flagellate Tetraselmis chui (strain PLY429) in the presence and absence of a community of bacterioplankton at two pH levels. Growth of PLY429 and total nutrient uptake were calculated for each treatment. The addition of bacterioplankton resulted in lower growth rates of PLY429, but the removal of ammonium was greater in those cultures with bacterioplankton present. The division rate of PLY429 was affected by pH; however, pH changes did not result in different uptake rates of nitrate, ammonium, or phosphate by the mixed algal and bacterial assemblage. These findings suggest that bacterioplankton and phytoplankton were competing for ammonium and that a lower pH resulted in more rapid algal growth. Mention of a trade name does not imply endorsement by the National Marine Fisheries Service.     

Tree allometry of Douglas fir and Norway spruce on a nutrient-poor and a nutrient-rich site

Research related to the allometric relationships of tree height and projected tree crown area to diameter at breast height was conducted to look at the biological suitability and timber production potential of Douglas fir under the conditions present in central Europe. The dependence of allometric relationships on soil nutrient conditions were described in forest stands of Douglas fir and Norway spruce. The studied sites were climatically similar but differed in soil nutrient availability. A significant difference was found in the allometric relationships of Norway spruce trees from the nutrient poor and nutrient rich site. In contrast to the Norway spruce, there was no significant effect of site fertility on allometric relationships for Douglas fir suggesting that its allocation patterns were less sensitive to site nutrient conditions. Stem growth increment, which was measured weekly during two consecutive seasons for both species, was related to the weather conditions and available soil moisture. Stem growth of Douglas fir began about 2 weeks earlier than in the Norway spruce at both sites. At the nutrient rich site, most of the stem growth of both species occurred at the beginning of the season, while growth at the other site was more evenly distributed throughout the season. Data obtained in this study will be useful for modeling stem growth and analysis of water use efficiency of these two tree species.     

Species-specific phytoplankton responses to nutrients and zooplankton manipulations in enclosure experiments

1. In situ enclosure experiments were performed in the mesotrophic Bermejales reservoir to evaluate the algal response to changes in the nutrient supply and in the zooplankton size structure and density in a 2 × 2 factorial design. The experiments were conducted during the spring bloom of nanoplanktonic diatoms in 1989. 2. Nutrient enrichment promoted a great increase of phytoplankton biomass indicating a strong nutrient limitation on phytoplankton growth. Total phytoplankton biomass was significantly lower in the Daphina-added enclosures at a given nutrient level and strong direct an indirect effect of zooplankton on phytoplankton community structure and nutrient availability were observed. 3. Most of the nanoplanktonic species were effectively grazed but species with protective coverings and large size colonies were favoured by grazers and small chlorococcales were unaffected probably because of their compensatory high growth rates. The decrease in total biomass imposed by grazers is attributable mainly to the decrease of Cyclotella ocellata, the most abundant species. This taxon suffers two net effects of zooplankton: direct grazing and the indirect decrease of Si availability caused by the growth of C. ocellata which was promoted by P excretion by zooplankton. Indirect effects of grazers on Si availability should, therefore, be taken into account in explaining phytoplankton succession and community structure. 4. In this experiment grazers affected considerably the nanoplanktonic community in Bermejales reservoir. The extent which they were affected, however, depended not only on the algal size as a determinant of edibility but also greatly on the specific nutrient requirements and taxonomic features of the algal species.     

SIZE-DEPENDENT PHOSPHORUS UPTAKE KINETICS AND CELL QUOTA IN PHYTOPLANKTON1

The allometric equation, y = aX^b, described the interspecific variation of phosphate uptake kinetics and cell quota with phytoplankton cell size and showed that smaller cells are superior in uptake rate to large. Species-specific measurements, made by track autoradiography in phosphorus deficient cultures of communities from a phosphorus-limited lake, revealed that eight different species did not differ significantly in the Michaelis-Menten half-saturation constant, K_m. However, both saturated uptake rates (V_max) and the initial slope of the uptake curve (V_max:K_m) decreased per unit biomass with increasing cell size. Biomass-specific cell phosphorus quotas also decreased with increasing cell volume, but less rapidly than did V_max or V_max: K_m. Comparable data from the literature showed that marine species were superior in phosphorus uptake to freshwater species of similar size, but allometric variation of kinetics appeared to exist within both groups. Together with a variable internal stores model of phosphorus-limited growth, the allometric relationships of uptake kinetics and quotas predicted competition to favor smaller cells, with a differential in growth rate diminishing as competitive intensity increased.     

Harmful algal blooms of allelopathic microalgal species: The role of eutrophication

The ability of certain harmful algal species to produce and release chemicals that inhibit the growth of co-occurring phytoplankton species, here considered as allelopathy, is closely associated with competition for limiting nutrient resources. Many phytoplankton cells are known to release elevated amounts of organic compounds under nutrient limitation. Eutrophication alters the nitrogen-to-phosphorus balance and, when nutrient availability is unbalanced, nutrient limitation may result. Algal species that can compete successfully for available growth-limiting nutrient(s) have the potential to become dominant and form blooms. The stress conditions imposed by the shifted nutrient supply ratios can, in some algae, stimulate production of allelochemicals that inhibit potential competitors. Thus, under cultural eutrophication, altered nutrient (N, P) ratios and limiting nutrient supplies can stimulate increased production of allelochemicals, including toxins, by some algal species and accentuate the adverse effects of these substances on other algae. Future investigation on the characterization of the chemical compounds involved in the allelopathic process are needed to advance the study of the mode of action of phytoplankton allelochemicals.     

Growth rate variation among passerine species in tropical and temperate sites: an antagonistic interaction between parental food provisioning and nest predation risk

Causes of interspecific variation in growth rates within and among geographic regions remain poorly understood. Passerine birds represent an intriguing case because differing theories yield the possibility of an antagonistic interaction between nest predation risk and food delivery rates on evolution of growth rates. We test this possibility among 64 Passerine species studied on three continents, including tropical and north and south temperate latitudes. Growth rates increased strongly with nestling predation rates within, but not between, sites. The importance of nest predation was further emphasized by revealing hidden allometric scaling effects. Nestling predation risk also was associated with reduced total feeding rates and per-nestling feeding rates within each site. Consequently, faster growth rates were associated with decreased per-nestling food delivery rates across species, both within and among regions. These relationships suggest that Passerines can evolve growth strategies in response to predation risk whereby food resources are not the primary limit on growth rate differences among species. In contrast, reaction norms of growth rate relative to brood size suggest that food may limit growth rates within species in temperate, but not tropical, regions. Results here provide new insight into evolution of growth strategies relative to predation risk and food within and among species.     

Tests of autotrophic picoplankton as early indicators of nutrient enrichment in an ultra-oligotrophic lake

1. The potential of picocyanobacteria as early indicators of changes in nutrient loading and trophic status was examined in an ultra-oligotrophic lake.
2. The study consisted of in situ, short-term, nutrient-addition bioassays and surveys of picocyanobacterial variables and other indices of trophic state at six sites selected to include a range of localized nutrient loadings to the lake from its catchment. The bioassays and surveys were conducted six times throughout 1 year.
3. Experimental additions of small amounts of ammonium-N and phosphate-P did not stimulate picocyanobacterial growth, and phosphate additions often reduced picocyanobacterial growth rates.
4. A correlation analysis using pooled data from all sites and sampling dates showed that the abundance of aggregated picocyanobacteria was strongly correlated with nutrient concentration and ratios. Other variables, including the concentration of single-cell picocyanobacteria, chlorophyll a and primary production, were poorly correlated with nutrients.
5. The results show that picocyanobacteria in oligotrophic lakes are sensitive to extremely small changes in nutrient availability and that they can respond in complex ways. The mechanisms by which they respond to such changes require further study before they can be used as bio-indicators of nutrient enrichment.     

Growth characteristics and growth modeling of <Emphasis Type="Italic">Microcystis aeruginosa</Emphasis> and <Emphasis Type="Italic">Planktothrix agardhii</Emphasis> under iron limitation

Although iron is a key nutrient for algal growth just as are nitrogen and phosphorus in aquatic systems, the effects of iron on algal growth are not well understood. The growth characteristics of two species of cyanobacteria, Microcystis aeruginosa and Planktothrix agardhii, in iron-limited continuous cultures were investigated. The relationships between dissolved iron concentration, cell quota of iron, and population growth rate were determined applying two equations, Monod’s and Droop’s equations. Both species produced hydroxamate-type siderophores, but neither species produced catechol-type siderophores. The cell quota of nitrogen for both M. aeruginosa and P. agardhii decreased with decreasing cell quota of iron. The cell quota of phosphorus for M. aeruginosa decreased with decreasing cell quota of iron, whereas those for P. agardhii did not decrease. Iron uptake rate was measured in ironlimited batch cultures under different degrees of iron starvation. The results of the iron uptake experiments suggest that iron uptake rates are independent of the cell quota of iron for M. aeruginosa and highly dependent on the cell quota for P. agardhii. A kinetic model under iron limitation was developed based on the growth characteristics determined in our study, and this model predicted accurately the algal population growth and iron consumption. The model simulation suggested that M. aeruginosa is a superior competitor under iron limitation. The differences in growth characteristics between the species would be important determinants of the dominance of these algal species.     

Jellyfish Body Plans Provide Allometric Advantages beyond Low Carbon Content

Jellyfish form spectacular blooms throughout the world’s oceans. Jellyfish body plans are characterised by high water and low carbon contents which enables them to grow much larger than non-gelatinous animals of equivalent carbon content and to deviate from non-gelatinous pelagic animals when incorporated into allometric relationships. Jellyfish have, however, been argued to conform to allometric relationships when carbon content is used as the metric for comparison. Here we test the hypothesis that differences in allometric relationships for several key functional parameters remain for jellyfish even after their body sizes are scaled to their carbon content. Data on carbon and nitrogen contents, rates of respiration, excretion, growth, longevity and swimming velocity of jellyfish and other pelagic animals were assembled. Allometric relationships between each variable and the equivalent spherical diameters of jellyfish and other pelagic animals were compared before and after sizes of jellyfish were standardised for their carbon content. Before standardisation, the slopes of the allometric relationships for respiration, excretion and growth were the same for jellyfish and other pelagic taxa but the intercepts differed. After standardisation, slopes and intercepts for respiration were similar but excretion rates of jellyfish were 10× slower, and growth rates 2× faster than those of other pelagic animals. Longevity of jellyfish was independent of size. The slope of the allometric relationship of swimming velocity of jellyfish differed from that of other pelagic animals but because they are larger jellyfish operate at Reynolds numbers approximately 10× greater than those of other pelagic animals of comparable carbon content. We conclude that low carbon and high water contents alone do not explain the differences in the intercepts or slopes of the allometric relationships of jellyfish and other pelagic animals and that the evolutionary longevity of jellyfish and their propensity to form blooms is facilitated by their unique body plans.     

Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore

The partial pressure of carbon dioxide (pCO₂) in lake ecosystems varies over four orders of magnitude and is affected by local and global environmental perturbations associated with both natural and anthropogenic processes. Little is known, however, about how changes in pCO₂ extend into the function and structure of food webs in freshwater ecosystems. To fill this gap, we performed laboratory experiments using the ecologically important planktonic herbivore Daphnia and its algal prey under a natural range of pCO₂ with low light and phosphorus supplies. The experiment showed that increased pCO₂ stimulated algal growth but reduced algal P : C ratio. When feeding on algae grown under high pCO₂, herbivore growth decreased regardless of algal abundance. Thus, high CO₂‐raised algae were poor food for Daphnia. Short‐term experimental supplementation of PO₄ raised the P content of the high CO₂‐raised algae and improved Daphnia growth, indicating that low Daphnia growth rates under high pCO₂ conditions were due to lowered P content in the algal food. These results suggest that, in freshwater ecosystems with low nutrient supplies, natural processes as well as anthropogenic perturbations resulting in increased pCO₂ enhance algal production but reduce energy and mass transfer efficiency to herbivores by decreasing algal nutritional quality.     

Allometric and trait‐based patterns in parasite stoichiometry

We measured the elemental content (%C, N and P) and ratios (C:N, C:P, N:P) of a diverse assemblage of parasitic helminths to ask whether taxonomy or traits were related to stoichiometric variation among species. We sampled 27 macroparasite taxa, spanning four phyla, infecting vertebrate and invertebrate hosts from freshwater ecosystems in New Jersey. Macroparasites varied widely in elemental content, exhibiting 4.7‐fold variation in %N, 4.6‐fold variation in %P, and 11.5‐fold variation in N:P. Across all species, parasite %P scaled negatively and C:P scaled positively with body size. Similar relationships between parasite P content and body size occurred at the phylum level and within individual species. The allometric scaling of P across species supports the growth rate hypothesis, which predicts that smaller taxa require more P to support relatively higher growth rates. Life cycle stage was related to %N and C:N, with non‐reproductive parasite stages lower in %N and higher in C:N than actively reproducing parasites. Parasite phylum, functional feeding group, and trophic level did not explain elemental variation among species. Organismal stoichiometry is linked to ecological function, and wide variation in macroparasite stoichiometry likely generates diverse patterns in host–parasite nutrient dynamics and variable relationships between parasitism and nutrient cycling.     

Nutrient uptake in eastern deciduous tree seedlings

Tree seedlings that colonize large treefall gaps are generally shade-intolerant species with high potential relative growth rates. Nutrient availability may be significantly elevated in disturbance-induced gaps, however, little is known about the role of differences in nutrient uptake capacities of different species in structuring the community response to gap openings in eastern North American deciduous forests. Seven tree species were grown from seed under both a high and a low nutrient regime, and uptake kinetics of phosphate, ammonium, and nitrate were studied. Yellow birch, a species with intermediate shade tolerance and relative growth rate, had the highest maximum rates of uptake of all ions, while tulip tree, a gap-colonizing species with high relative growth rate, had the lowest rate of phosphate uptake and intermediate rates of ammonium and nitrate uptake. Beech and hickory, which have low relative growth rates and are not gap-colonizing species, had intermediate levels of nutrient uptake. There was no evidence that species with the highest maximum uptake rates measured at high supply concentrations had relatively low uptake at low nutrient supply concentrations. Although birch increased phosphate absorption capacity when grown under a low nutrient regime, this pattern did not hold for nitrate or ammonium uptake, and other species showed no change in nutrient uptake capacity according to nutrient growth regime. Clearly, factors other than nutrient absorption capacity, such as nutrient use efficiency or allocation to root vs. shoot biomass, underlie differences in species' capacities to colonize and maintain a high relative growth rate in canopy gaps.     

Cell size is positively correlated between different tissues in passerine birds and amphibians,but not necessarily in mammals

We examined cell size correlations between tissues, and cell size to body mass relationships in passerine birds, amphibians and mammals. The size correlated highly between all cell types in birds and amphibians; mammalian tissues clustered by size correlation in three tissue groups. Erythrocyte size correlated well with the volume of other cell types in birds and amphibians, but poorly in mammals. In birds, body mass correlated positively with the size of all cell types including erythrocytes, and in mammals only with the sizes of some cell types. Size of mammalian erythrocytes correlated with body mass only within the most taxonomically uniform group of species (rodents and lagomorphs). Cell volume increased with body mass of birds and mammals to less than 0.3 power, indicating that body size evolved mostly by changes in cell number. Our evidence suggests that epigenetic mechanisms determining cell size relationships in tissues are conservative in birds and amphibians, but less stringent in mammals. The patterns of cell size to body mass relationships we obtained challenge some key assumptions of fractal and cellular models used by allometric theory to explain mass-scaling of metabolism. We suggest that the assumptions in both models are not universal, and that such models need reformulation.     

Effects of temporal and spatial heterogeneities created by consumer-driven nutrient recycling on algal diversity

A spatially explicit plant-herbivore model composed of planktonic herbivores, algal preys and nutrients was constructed to examine the effects of consumer-driven nutrient recycling (CNR) on the algal species richness with and without spatial structure. The model assumed that either of two essential nutrients (N and P) limited growth of algal populations and that consumer individuals moved randomly in the lattice and grazed all the algal species with the same efficiency. The results showed that when there was no CNR, the number of persistent algal species was affected by neither supply rates of external nutrients nor spatial structure and was consistently low. When consumers recycled nutrients according to their stoichiometry, the algal species richness changed with supply rates of external nutrients depending on spatial structure: the algal species richness decreased with increasing nutrient loadings when there were no spatial structure because CNR increased the probability of stochastic extinction of algal species by amplifying the oscillation of algae-consumer dynamics. However, when spatial structures were created by the migration of consumers, CNR increased the algal species richness in a range of nutrient loadings because spatial variation of grazing pressure functioned to stabilize the algal-consumer dynamics. The present study suggests that through grazing and nutrient recycling, consumer individuals can create ephemeral heterogeneity in growth environments for algal species and that this ephemerality is one of the keys to understanding algal species in nature.     

Causes of variation in wing loading among Drosophila species

We examined influences on wing and body size in 11 species (12 strains) of Drosophila. Six measures of wing length and width were closely correlated with wing area and suggested little variation in wing shape among the species. Among ten species wing loading, an important factor in flight costs and manoeuvrability, increased as body mass increased at a rate consistent with expectations from allometric scaling of wing area and body mass to body length. Intraspecific variation in wing loading showed similar relationships to body mass. Density and temperature during larval development influenced wing loading through general allometric relations of body size and wing area. Temperature during the pupal stage, but not during wing hardening after eclosion, influenced wing area independently of body size. Wing area increased as growth temperature decreased. Individuals reared at cooler temperatures thus compensated for a potential allometric increase in wing loading by differentially enlarging the wing area during pupal development.     

On the vegetative biomass partitioning of seed plant leaves, stems, and roots

A central goal of comparative life-history theory is to derive the general rules governing growth, metabolic allocation, and biomass partitioning. Here, we use allometric theory to predict the relationships among annual leaf, stem, and root growth rates (GL, GS, and GR, respectively) across a broad spectrum of seed plant species. Our model predicts isometric scaling relationships among all three organ growth rates: GL is proportional to GS is proportional to GR. It also provides a conceptual basis for understanding the differences in the absolute amounts of biomass allocated to construct the three organ types. Analyses of a large compendium of biomass production rates across diverse seed plant species provide strong statistical support for the predictions of the theory and indicate that reproductive investments may scale isometrically with respect to vegetative organ growth rates. The general rules governing biomass allocation as indexed by the scaling exponents for organ growth rates are remarkably indifferent to plant size and taxonomic affiliation. However, the allometric "constants" for these relationships differ numerically as a function of phenotypic features and local environmental conditions. Nonetheless, at the level of both inter- and intraspecific comparisons, the same proportional biomass allocation pattern holds across extant seed plant species.     

Rejection of non-adaptive hypotheses for intraspecific variation in trophic morphology in gape-limited predators

Recent studies have interpreted intraspecific divergence in relative head sizes in snakes as evidence for adaptation of the trophic apparatus in gape-limited predators to local prey size. However, such variation might also arise from non-adaptive processes (such as allometry, correlated response, genetic drift, or non-adaptive phenotypic plasticity). We test predictions from these alternative hypotheses using data on the allometric relationship between head size and body size in two wide-ranging snake species: eight populations of adders ( Vipera berus ) and 30 populations of common gartersnakes ( Thamnophis sirtalis ). Our data enable strong rejection of the alternative (non-adaptive) hypotheses, because the relationship between head and body size differed significantly among populations, the geographic distance separating pairs of populations explained less than 1.5% of their divergence in allometric coefficients, and the within-population allometric coefficients were higher than the among-population coefficients in each species. In addition, the geographical variability of allometric coefficients in females did not parallel that in males, suggesting that allometric coefficients have evolved independently in the two sexes. Phenotypic plasticity also cannot explain the data, because laboratory studies show that the allometric relationship between head size and body size is relatively insensitive to differing growth rates. We conclude that the intraspecific head size divergence in these snakes is better explained by spatially heterogeneous selection to optimize prey handling ability, than by non-adaptive processes.     

Relative brain size,stratification, and social structure in anthropoids

The relationships between relative brain size and both stratification and social structure were examined in a total of 82 species of anthropoids. The species were divided into a total of 42 congeneric groups which consisted of congeneric species with similar ecologies and social structures. The relative brain size (RBS) was calculated for each congeneric group in each superfamily, based on an allometric equation describing the relationship between brain weight and body weight for each superfamily. Among congeneric groups with a common category of diet, RBS was significantly greater for terrestrial groups than for arboreal groups, and for polygynous (i.e. multi-female) groups than for monogynous (single-female) groups. Furthermore, RBS was significantly and positively correlated with the size of the home range per individual for the Cercopithecoidea, and with troop size for frugivorous groups of the Ceboidea. The results obtained suggest that factors associated with terrestriality and polygyny have been involved in the increases in relative brain size of anthropoids.