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Abstracts
of Recent Publications,
VIMS Evolutionary Ecology Lab

Duffy, J.E. and A.M. Harvilicz. (in revision). Species-specific impacts of grazing amphipods in an eelgrass-bed community. Marine Ecology Progress Series.

Small, grazing invertebrates often benefit seagrasses by cropping their epiphytic algal competitors.  Yet predictive relationships between grazer abundance and seagrass performance remain elusive, in significant part because of poorly understood diversity in mesograzer feeding biology.  We conducted experiments in eelgrass (Zostera marina) microcosms to explore how differences in feeding between two common grazing amphipod taxa affected accumulation and species composition of epiphytes on eelgrass, as well as amphipod population growth, competition, and production, over a four-week period in summer.  Gammarus mucronatus and ampithoids (a mixture of Cymadusa compta and Ampithoe longimana) were stocked, singly and in combination, along with a grazer-free control treatment.  Amphipod population growth rates indicated that the two taxa competed for a common limiting resource, presumably periphyton, which was essentially eliminated in all grazer treatments.  Final abundances of both amphipod taxa were 53-68% lower in treatments where the other grazer was present than in single-species grazer treatments.   A common carrying capacity was also indicated by the nearly identical final biomass of amphipods across treatments, despite two-fold variation in initial amphipod densities.  These results support the hypothesis that the two amphipod taxa are roughly equivalent in terms of resource requirements and production rates.  Despite this equivalence, subtle differences in diet breadth between amphipod taxa translated into substantial differences in biomass and composition of the fouling assemblage among treatments.  Whereas grazer-free eelgrass became heavily fouled with periphyton and tunicates, eelgrass exposed to G. mucronatus alone was overgrown by the red alga Polysiphonia harveyi, which reached a biomass equal to the total fouling mass in grazer-free controls.  P. harveyi was nearly absent in all other treatments.  In contrast, eelgrass with ampithoids was virtually devoid of all fouling material.  Thus, similar mesograzer species can have markedly different impacts on fouling assemblages, and these occur despite strong similarity in grazer energetics and primary food sources.  Our results may help to reconcile evidence of diet overlap and diffuse competition among mesograzer species with the different feeding preferences and community impacts demonstrated for several mesograzers in experimental studies.

Plant diversity is believed to govern animal community structure, yet few have tested this relationship.  We manipulated plant species diversity and composition (two seagrasses and three seaweeds) and measured the abundance, diversity, and biomass of plant-associated macroinvertebrates.  Animal diversity was weakly but positively related to plant diversity (Simpson’s 1- lambda).  Most indices of animal diversity, however, were more strongly related to total plant surface area than to plant diversity.  Epifaunal abundance and biomassincreased, whereas epifaunal diversity and evennessdecreased with total plant surface area.  Both food and habitat covary with plant surface area, providing potential mechanistic explanations for these patterns.

Plant species composition had strong effects on epifaunal community structure.  After statistically controlling for effects of plant surface area, epifaunal abundance and biomass remained higher, and evenness remained lower, among assemblages composed of branched (mostly seaweeds) relative to unbranched (mostly seagrasses) macrophytes.  Multiple regression analyses also revealed differential use of particular plant species by epifauna.  For example, amphipods responded particularly strongly to the coarsely-branched red alga Gracilaria verrucosa.  Thus, our experimental results support a strong effect of plant species composition, and little effect of plant diversity per se, on the motile macrofauna that we studied.  This conclusion is consistent with results of a concurrent field survey; epifaunal community structure differed among plant species and seasons, with no host-plant specialists.  These results support evidence from both terrestrial and aquatic communities; ecosystem structural and functional properties are often more strongly influenced by the particular attributes, rather than the number of species, in a community.

Concern over the accelerating loss of biodiversity has stimulated renewed interest in relationships between species richness, species composition, and the functional properties of ecosystems.  Mechanistically, the degree of functional differentiation or complementarity among individual species determines the form of diversity/function relationships and is thus important to distinguishing among alternative hypotheses for the effects of species richness on ecosystem processes.  Although a growing number of studies has reported relationships between plant species richness and ecosystem processes, few have explicitly addressed how diversity at higher trophic levels influences functional processes.  We used mesocosms to test experimentally the impacts of three herbivorous crustacean species on plant biomass accumulation, relative dominance of plant functional groups, and herbivore secondary production in beds of eelgrass (Zostera marina), a dominant feature of shallow estuaries throughout the northern hemisphere.  By establishing treatments with each of the grazer species alone and in combination, we tested the degree of functional redundancy among grazer species and the relationship between grazer species richness and productivity.

Grazer species composition strongly influenced eelgrass biomass accumulation and grazer secondary production, whereas none of the processes we studied was clearly related to grazer species richness.  In fact, all three measured ecosystem processes — epiphyte, eelgrass, and grazer biomass accumulation — reached highest values in particular single-species treatments.  Experimental deletions of individual species from the otherwise intact assemblage confirmed that the three grazer species were functionally redundant in impacting epiphyte accumulation, whereas both eelgrass shoot/root ratio and secondary production were sensitive to deletion of certain grazer species, indicating unique roles of particular grazers in influencing these variables.  In the field, seasonal abundance patterns differed markedly among the dominant grazer species, suggesting that complementary grazer phenologies may reduce total variance in grazing pressure on an annual basis.  Preliminary results indicate that interspecific competition may explain the lower rates of grazing we found in multi-species grazer assemblages.  Our results show that even superficially similar species can differ substantially in their impacts on ecosystem processes and emphasize caution in assuming redundancy when assigning species to functional groups.

Duffy, J.E. and M.E. Hay.  2000.  The ecology and evolution of marine consumer-prey interactions. Pages 131-157 in: M.D. Bertness, M.E. Hay, and S.D. Gaines, editors. Marine Community Ecology. Sinauer Associates, Sunderland, MA.

Consumer pressure is a pervasive influence on the evolution of populations and on the structure and function of nearly all marine communities and ecosystems.  Studies conducted throughout temperate and tropical seas have shown that removal of herbivores or predators often produces profound changes in community organization, habitat structure, and ecosystem processes.  The rise of humans as apex predators in an expanding range of marine (and terrestrial) habitats is similarly producing cascading impacts in both benthic and pelagic systems worldwide.  Prey organisms may persist in the face of consumer pressure by escaping their consumers in time or space, by tolerating limited tissue loss to consumers, and/or by deterring consumers.  Escape may be achieved through migration, rapid growth, other life history adaptations, or associations with defended neighbors.  Tolerance often involves rapid growth or protection of reproductive structures in tissues inaccessible to consumers.  Deterrence takes a wide array of forms, from deployment of diverse chemical compounds through various forms of structural armor.  The generally positive association in time and space between intense consumer pressure and well-developed defenses implies that such defenses are costly to the prey and are selected against where consumer pressure is low.  This cost hypothesis is supported by several experimental studies of phenotypically plastic or polymorphic species.  In evolutionary time, consumers are important selective agents, molding the behavior, morphology, chemistry, and life history of prey organisms, particularly in the tropics where consumer pressure is especially intense.  Many specific, and even obligate, associations between defended marine host species and undefended guest species appear to have evolved in response to intense predation pressure on the guest.  Several unresolved issues deserve more attention in marine consumer-prey studies: What characteristics of organism and environment predispose a consumer to have strong ("keystone") impacts on a community?  Does the strength of consumer impacts in a system vary predictably as a function of community structure (species diversity, food chain length, etc.) or abiotic variables (physical energy, nutrient flux)?  How do the results of typical experimental manipulations of marine communities scale up to broader scales in time and space, and how will evolutionary change and species turnover affect patterns seen in small-scale experiments?  Answering such questions will be critical if we hope to predict, plan for, and mitigate the accelerating effects of global change on marine ecosystems.

Epifaunal animals are a conspicuous and ecologically important component of some estuaries where low oxygen events (dissolved oxygen concentration in the water column < 2 mg O2 l-1), termed hypoxia, are common.  Although hypoxia is increasing in frequency and intensity in many estuaries, and is known to have adverse impacts on many infaunal organisms, little is known regarding its effects on epifauna.  We characterized the abundance and species composition of sessile and mobile epifaunal assemblages in the York River, a tributary of the Chesapeake Bay, USA, during the summer hypoxia seasons in 1996 and 1997.  We collected communities on artificial substrates in two areas of the river that have historically experienced different exposure to hypoxia.  Despite frequent hypoxic stress, epifauna formed dense communities in both areas.  Dominant species comprised a range of phyla and included the polychaetes Polydora cornuta and Sabellaria vulgaris, the bryozoans Membranipora tenuis and Conopeum tenuissimum, the tunicate Molgula manhattensis, the barnacle Balanus improvisus, the anemone Diadumene leucolena and the hydroids Ectopelura dumortieri and Obelia bicuspidata.  Common mobile species included the nudibranchs Cratena kaoruae and Doridella obscura, the amphipods Melita nitida and Paracaprella tenuis, the polychaete Nereis succinea and the flatworm Stylochus ellipticus.  We found few differences in species composition between the two areas, even though one area usually experienced lower oxygen concentrations during hypoxic events, suggesting that hypoxia does not exclude any epifaunal species in the York River.  We did find differences between the two study areas in percent cover and abundance of some species.  While tunicates, hydroids and anemones were equally abundant in both areas during both study years, bryozoans and the polychaete S. vulgaris were more abundant in the area with generally higher oxygen, suggesting that they may be less tolerant of hypoxic stress.  The polychaete P. cornuta was more abundant in the area that usually had lower oxygen.  These results suggest that many epifaunal species have high hypoxia tolerance, and most epifaunal species found in the lower York River are able to survive in hypoxic areas.  We conclude that, in contrast to earlier predictions, epifaunal species are not necessarily more susceptible to hypoxia than infaunal species in the York River.  Epifaunal communities in areas with brief hypoxic episodes and moderate hypoxia (0.5 - 2 mg O2 l-1) can persist with little change in species composition, and with few changes in abundance, as oxygen concentrations fall.

As the most extreme expression of apparent altruism in nature, eusociality has long posed a central paradox for behavioral and evolutionary ecology. Because eusociality has arisen rarely among animals, understanding the selective pressures important in early stages of its evolution remains elusive. Employing an historical approach to this problem, we used morphology and DNA sequences to reconstruct the phylogeny of 13 species of sponge-dwelling shrimps (Synalpheus) with colony organization ranging from asocial pair-bonding through eusociality. We then used phylogenetically independent contrasts to test whether sociality was associated with evidence of enhanced competitive ability as suggested by hypotheses invoking an advantage of cooperation in crowded habitats. The molecular, morphological, and combined data each strongly supported three independent origins of monogynous, multigenerational (eusocial) colony organization within this genus. Phylogenetically independent contrasts confirmed that highly social taxa, with strong reproductive skew, have significantly higher relative abundance within the host sponge than do less social taxa, a result that was robust to uncertainty in tree topology and varying models of character change. A similar tendency for highly social species to share their sponge with fewer congener species was suggestive but not significant. Because unoccupied habitat appears to be limiting for many sponge-dwelling shrimp species, these data are consistent with hypotheses that cooperative social groups enjoy a competitive advantage over less organized groups or individuals where independent establishment is difficult, and that enemy pressure is of central importance in the evolution of animal sociality.

Large brown seaweeds dominate coastal hard substrata throughout many of the world's oceans. In coastal North Carolina, USA, this dominance by brown seaweeds is facilitated by omnivorous fishes, which feed both on red and green algae and on herbivorous amphipods that graze brown algae. When fish are removed in the field, brown seaweeds are replaced by red seaweeds, and herbivorous amphipods appear more abundant. Using an array of large (~4000 L), outdoor mesocosms, we tested three mechanistic hypotheses for this pattern: fish feeding facilitates brown algal dominance (1) by removing red and green algal competitors, (2) by removing amphipods and reducing their feeding on brown seaweeds, or (3) through an interaction of these mechanisms. Our experiments revealed strong impacts of both fish and amphipods, and a key role for the interaction, in structuring this community. When both fish and amphipods were removed (the latter with dilute insecticide), space was rapidly dominated and held for 17 weeks by fast-growing, primarily filamentous green algae. In contrast, when either fish, amphipods, or both were present, green algae were cropped to a sparse turf and space was more rapidly dominated by larger macroalgae. The impacts of amphipods and fish on late- successional macroalgal assemblages were comparable in magnitude, but different in sign: red seaweeds prevailed in the amphipod-dominated treatment, whereas browns dominated in the presence of fish. Laboratory feeding assays, and amphipod densities in the tanks, suggested that the significant effects of amphipods were attributable largely, if not exclusively, to the single amphipod species Ampithoe longimana, which fed heavily on brown macroalgae. Our experimental removal of red and green algae failed to enhance cover of brown algae significantly; however, the latter reached substantially lower cover in the grazer-removal treatment, where green algae were very abundant, than in the fish-only treatment where green algae were sparse. Thus, our results support the third hypothesis: fish-mediated dominance of brown algae involves both suppression of grazing amphipods and removal of algal competitors. Although collective impacts of fish and amphipods on this benthic community were generally comparable in magnitude, impacts normalized to each grazer's aggregate biomass were consistently higher for amphipods than for fish, sometimes by 1-2 orders of magnitude. Thus, the impacts of grazing amphipods (specifically A. longimana) on the benthic community were both strong and disproportionate to their biomass. These experimental results imply that grazing amphipods, which are ubiquitous in marine vegetation but poorly understood ecologically, may play important roles in the organization of benthic communities, particularly where predation pressure is low.

A new species of Synalpheus is described based on specimens collected from sponges in Belize and the Atlantic coast of Panama. The new species, Synalpheus williamsi, is most similar morphologically to S. goodei Coutière, but the two species are consistently different in several morphological and larval features, and occupy distinct species of sponges. The shape of the major chela and of the uropodal exopods are the most reliable morphological characters that distinguish the two species. The first larval stage, a zoea I, was obtained from an ovigerous female of the new species. The zoea I is similar to that of S. neomeris (De Man), S. triunguiculatus (Paulson), S. tumidomanus (Paulson), and S. scaphoceris Coutière, in lacking pleopods and chelae, but can be distinguished by the presence of an acute projection on the pterygostomian corner.

Several species of sponge-dwelling alpheid shrimps (Synalpheus) appear to exhibit unusual colony organizations reminiscent of those found in social insects, but few of these shrimp species have been studied in detail. We sampled colonies of S. filidigitus Armstrong, 1949 from its two main hosts, the sponges Oceanapia sp. and Xestospongia spp., at Carrie Bow Cay, Belize. Colonies contained all size classes of shrimp, from recent hatchlings to mature, brooding females. The majority of colonies consisted of <30 individuals, although a few reached much larger sizes (maximum = 94 in Oceanapia and 121 in Xestospongia). In all but one of the sampled colonies containing mature female(s), only a single female (the "queen") was present. Distinct cohorts of juveniles, apparently produced by the resident female, were recognizable in several colonies, and the total number of individuals in the colony was strongly correlated with the resident female's size and fecundity. These observations suggest that, as previously shown for the eusocial S. regalis, the colony is a close kin group consisting mainly of the queen's philopatric offspring. Comparison of females from a range in colony sizes revealed an apparent ontogenetic transformation in the queen's morphology: whereas smaller (presumably younger) females were morphologically similar to males, queens from larger colonies were considerably larger than males, had proportionally longer and wider abdomens, and the massive major chela of the first pereiopod was replaced with a small chela identical to the normal minor first chela. Colonies of S. filidigitus are quite similar in organization to those of S. regalis, suggesting that S. filidigitus may be eusocial according to the traditional definition, and bringing to three the number of Synalpheus species reported to exhibit this paradoxical social organization.

Abstract: Recently, the Caribbean snapping shrimp Synalpheus regalis was shown to be eusocial by the criteria historically used for honeybees, ants, and termites, i.e., colonies contain a single reproducing female and a large number of non-breeding "workers". This finding prompted a reexamination of several previously puzzling reports of unusual population structures in other Synalpheus species. New collections, and observations made by students of this genus over the last century, suggest that several sponge-dwelling Synalpheus species similarly exhibit overlapping generations and monopolization of reproduction by a few individuals, and thus that these species may also be eusocial according to classical entomological criteria. The evidence for this conclusion includes reports of several Caribbean and Indo-Pacific species occurring in large aggregations of "juvenile" shrimp accompanied by few or no mature females. Here I describe one of these species as Synalpheus chacei. Like other members of the gambarelloides species group within this genus, S. chacei is an obligate inhabitant of living demosponges, and has been collected from at least seven host species in Caribbean Panama, Belize, and the Virgin Islands. Stomach contents comprised primarily detritus and diatoms, suggesting that S. chacei feeds on material inhaled in the host sponge's feeding current. The new species is morphologically similar to S. bousfieldi, and is most reliably distinguished from it (and indeed, apparently from all other species of Synalpheus) by a unique pair of longitudinal setal combs on the dactyl of the minor first chela. Like S. regalis, S. chacei lives in colonies of up to several dozen individuals of overlapping generations, in which only a single female breeds, and is thus likely to be eusocial. Interestingly, males of S. chacei exhibit an apparent dimorphism in the development of the major chela (fighting claw) which may reflect a concomitant differentiation in behavior among individuals within a colony.

Duffy, J.E. 1996. Eusociality in a coral-reef shrimp. Nature 381:512-514.

Abstract: The apex of animal social organization is eusociality, characterized by three criteria: overlapping generations, reproductive division of labor, and cooperative care of young. To date, eusociality has been recognized only among social insects, and the celebrated African mole-rats. Here I report the first case of eusociality in a marine animal. The sponge-dwelling shrimp Synalpheus regalis lives in colonies of up to >300 individuals, each containing only a single reproductive female. Direct-developing juveniles remain in the natal sponge, and allozyme data suggest that most colony members are full sibs. In laboratory experiments, larger colony members, most of whom apparently never breed, defended the colony against heterospecific intruders. Striking similarities among sponge-dwelling shrimp, mole-rats, and termites — all diploid animals — strengthen arguments that eusociality is favored by gradual metamorphosis, parental care, and occupation of protected, expansible niches.

Duffy, J.E. 1996. Resource-associated population subdivision in a symbiotic coral-reef shrimp. Evolution 50:360-373.

Abstract. The importance of sympatric speciation remains controversial. An empirical observation frequently offerred in its support is the occurrence of sister taxa living in sympatry but using different resources. To examine the possibility of sympatric differentiation in producing such cases, I measured genetic, behavioral, and demographic differentiation between populations of the tropical sponge-dwelling shrimp Synalpheus brooksi occupying two alternate host species on three reefs in Caribbean Panama. This species belongs to an apparently monophyletic group of > 30 species of mostly obligate, host-specific sponge-dwellers, many of which occur in sympatry. Demographic data demonstrated the potential for disruptive selection imposed by the two host species: shrimp demes from the sponge Agelas clathrodes were consistently denser, poorer in mature females, more heavily parasitized by branchial bopyrid isopods, and less parasitized by thoracic isopods, than conspecific shrimp from the sponge Spheciospongia vesparium. Laboratory assays demonstrated divergence in host preference: shrimp on all three reefs tended to choose their native sponge species more often than did conspecific shrimp from the other host. Because S. brooksi mates within the host, this habitat selection should foster assortative mating by host species. A hierarchical survey of protein- electrophoretic variation also supported host-mediated divergence, revealing: 1) that shrimp from the two hosts are conspecific, as evidenced by absence of fixed allelic differences at any of nine allozyme loci scored, 2) strong genetic subdivision among populations of this philopatric shrimp on reefs separated by 1-3 km, and 3) significant host-associated genetic differentiation within two of the three reefs. Finally, intersexual aggression (a proxy for mating incompatibility) between shrimp from different host species was significantly elevated on the one reef where host- associated genetic differences were strongest, demonstrating concordance between genetic and behavioral estimates of divergence. Adjacent reefs appear to be semi-independent sites of host- associated differentiation, as evidenced by differences in the degree of host-associated behavioral and genetic differentiation, and in the specific loci involved, on different reefs. In philopatric organisms with highly subdivided populations, such as S. brooksi, resource-associated differentiation can occur independently in different populations, thus providing multiple "experiments" in differentiation, and resulting in a mosaic pattern of polymorphism as reflected by neutral genetic markers. Several freshwater fishes, an amphipod, and a snail similarly show independent but remarkably convergent patterns of resource-associated divergence in different conspecific populations, often in the absence of obvious spatial barriers. In each case, substantial differentiation has occurred in the face of continuing gene flow.

Duffy, J.E. 1996. Specialization, species boundaries, and the radiation of sponge-dwelling alpheid shrimp. Biological Journal of the Linnean Society 58:307-324.

Abstract: Microevolutionary studies and natural history suggest that host-specialization has promoted the high diversity of tropical sponge-dwelling snapping shrimps (Decapoda, Alpheidae, Synalpheus). Yet the taxonomic difficulty of this genus has precluded rigorous tests of this hypothesis. S. rathbunae Coutière is among the most abundant invertebrates inhabiting the framework of sponges and dead coral that forms the floor of Caribbean coral reefs. Even within a small area S. rathbunae exhibits the apparently wide variation in size, color, and morphology that has long frustrated efforts to identify and define species boundaries within this large (> 100 described species) genus. Here I show that sympatric populations of this nominal species occupying different sponge hosts display clear, concordant differences in allozyme genotypes and in multivariate morphometrics, confirming that the populations represent three distinct biological species. Moreover, careful field sampling revealed that the three S. rathbunae taxa and the closely related S. filidigitus Armstrong showed almost no overlap in the species of hosts occupied. Interestingly, while there was significant differentiation between Belizean and Panamanian populations of the one taxon that occurred at both sites (~1500 km apart), these populations were recognizable as conspecific using both genetic and morphological characters. These results show that 1) diversity of Synalpheus, which is already among the most species-rich crustacean genera, is probably several times higher than currently recognized, and 2) species of sponge-dwelling Synalpheus are highly host-specific, with related species distinctly segregated among hosts. Together with previous evidence of host race differentiation within shrimp species, these results suggest a primary role for resource specialization in the origin and/or maintenance of this group's characteristically high diversity.

Duffy, J.E. 1996. Synalpheus regalis, new species, a sponge-dwelling shrimp from the Belize Barrier Reef, with comments on host specificity in Synalpheus. Journal of Crustacean Biology 16:564-573.

Abstract: Synalpheus regalis (Decapoda: Alpheidae) is described from the demosponges Xestospongia cf. subtriangularis (Petrosiidae) and Hyattella intestinalis (Spongiidae) on the Belize Barrier Reef at Carrie Bow Cay. The new species is a member of Coutière's gambarelloides species group, and more specifically is one of a complex of morphologically very similar species, including S. rathbunae Coutière 1909, S. filidigitus Armstrong 1949, and at least one other undescribed species. Like most members of the gambarelloides group, S. regalis lives exclusively within the internal canals of living sponges, and at the type locality is found in only 2 of the 21 sponge species that harbor commensal shrimps. Such host specificity is typical of Caribbean Synalpheus species. The pattern of shrimp distribution among sponge species, and among individual sponges, suggests that suitable habitat at this site is saturated and that competition for living space is intense. The resulting restriction of Synalpheus species to those hosts in which they are competitively superior may thus be an important determinant of their characteristic host specificity.

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