Burrowing Mud Shrimp Research Articles

Occasional utilization of crustacean burrows by the estuarine goby Mugilogobius abei

Many species of gobies live in close association with various burrowing crustaceans. Mugilogobius abei is a common species distributed in a variety of estuarine environments from tidal pools in mudflats to tidal channels, even in polluted areas. This goby is usually found resting under pebbles, but gobies have been reported to use the burrows of upogebiid shrimp and brachyuran crabs as a shelter. This study aimed to describe the crustacean burrow use pattern of M. abei through both aquarium and field observations. In aquaria, we observed the behavior of the goby in the presence of burrowing mud shrimp Upogebia yokoyai or the crab Macrophthalmus banzai. A total of 19 out of 20 experimental individuals used shrimp burrows in the presence of the shrimp when the mud surface was covered with water. The goby entered and exited the burrows with bout durations of several seconds to over 10 s, and the goby spent 1–3% of the observation period in shrimp burrows. The goby used artificial crab burrows in much the same way in aquaria. In the field, we compared the shelters used by M. abei at two study sites where the availability of surface structures was different. The results showed that M. abei used crustacean burrows more often as a shelter in the habitat in which fewer surface structures were available. In summary, crustacean burrows are one of the items that can be used as shelters by goby, and their utilization patterns may vary depending on the characteristics of their habitat.

A review of three species of Hesperonoe (Annelida: Polynoidae) in Asia, with descriptions of two new species and a new record of Hesperonoe hwanghaiensis from Korea

ABSTRACTA taxonomic review of three Asian species of Hesperonoe (Annelida: Polynoidae) is presented. Hesperonoe hwanghaiensis Uschakov and Wu, 1959 (type locality: Qingdao, China) is redescribed based on five specimens collected from an intertidal site in the Korean coast of the Yellow Sea, as a new record of this species from Korea, which is the only known habitat outside the type locality. Hesperonoe coreensis sp. nov. is described based on nine specimens collected from two intertidal sites in the Korean coast of the Yellow Sea, including the same site as the habitat of H. hwanghaiensis. Hesperonoe japonensis sp. nov. is described by re-examination of many specimens collected from eight intertidal sites and a subtidal one in Japan, which was previously misidentified as H. hwanghaiensis. The three species are clearly distinguishable from one another by the species-specific morphology of the macrotubercles (or marked ridges) on the surface of elytra. All of the three species seemed to be commensal with the burrowing mud shrimp Upogebia major in intertidal flats, except for an additional probable host of another upogebid shrimp Austinogebia narutensis for H. japonensis sp. nov. in a subtidal habitat. The morphological characteristics and host species of the three Asian species are compared with all of the other five congeners known from the North American Pacific and Arctic Sea.http://www.zoobank.org/urn:lsid:zoobank.org:pub:51CB5C5B-0838-48AC-A0BA-8E63AA7628CB

Occurrence of Orthione griffenismarkham, 2004 (Isopoda: Bopyridae), parasite of the mud shrimp upogebia major(de Haan, 1841) in South Korean waters, and its implications with respect to marine bioinvasion

In recent years, extensive populations of burrowing mud shrimp have suddenly invaded the tidal flats in South Korea where clams, Ruditapes philippinarum, are harvested. These shrimp pose a serious threat to the clam industry along the west coast of South Korea. While conducting a mud shrimp monitoring program, we collected six female/male pairs of a pseudionine bopyrid isopod, Orthione griffenisMarkham, 2004, which in North America has been considered an introduced species from Asia that threatens northeastern Pacific estuarine ecosystems. We report the occurrence of this isopod as an inhabitant of the branchial chambers of the host shrimp, Upogebia major(de Haan, 1841), a very common species along the South Korean west coast, along with a morphological description and phylogenetic analysis based on COI barcodes. DNA analysis supported strongly that South Korean Orthioneis the same species of western Pacific (USA), O. griffenis. Two regionally disjunct isopods showed very low (0.8%) genetic variation in the mitochondrial COI (cytochrome oxidase subunit I) sequences. The implications of the occurrence of this species with respect to marine bioinvasion are also discussed.

Effects of the burrowing mud shrimp, Upogebia yokoyai, on carbon flow and microbial activity on a tidal flat

AbstractMud shrimps, Upogebia spp., are major constituents of macrobenthic communities in tidal flats in Japan. The impact of Upogebia yokoyai on carbon flow on tidal flats was examined by comparing CO2 emission rates from plots with and without burrows in the Kurose River estuary, Japan. In situ CO2 emission rates from plots with burrows were significantly higher than from those without. Laboratory measurements using sediment core samples that excluded respiration of macrobenthic organisms showed similar trends. Although there were no significant differences in grain size distribution, water content, or ignition loss between the sediment cores with and without burrows, oxidation–reduction potential was significantly higher in sediment cores with burrows. Analysis of phospholipid fatty acids (PLFA) indicated that microbial biomass and community structure did not differ significantly between cores with and without burrows. However, microbial respiration activity, as indicated by CO2 emission rates per total PLFA content, was significantly higher in sediment cores with burrows than in those without. Our results indicate that burrows of U. yokoyai change the physicochemical conditions and increase microbial activity in the sediment, significantly affecting carbon flow in the tidal flat.

AN OVERVIEW OF PREDATION EVIDENCE FOUND ON FOSSIL DECAPOD CRUSTACEANS WITH NEW EXAMPLES OF DRILL HOLES ATTRIBUTED TO GASTROPODS AND OCTOPODS

Predators of extant decapod crustaceans are fairly well known, but unlike many other invertebrate clades, not much is known regarding predation evidence found on fossil decapods. Herein, we provide an overview of such predation and expand upon this through an extensive study of fossil decapod specimens from multiple museum collections. Thus far most examples of predation come from drill holes and stomach contents; bite marks, incisions or irregular holes, and possible regurgitated material are also known. The currently recognized predators of decapods in the fossil record are fish, plesiosaurs, ammonites, octopods, and gastropods. We also provide new evidence of unambiguous drill-hole predation in decapods, based on 33,593 nonmoldic Cenozoic (middle Eocene– Holocene) decapod remains originating from Europe, Asia, and North America, indicating that drilling predation in decapods is more common than currently recognized. Drill holes attributed to octopods (ichnotaxon Oichnus ovalis) and gastropods (O. simplex and O. paraboloides) were found in carapaces and appendages from the Pliocene of the Netherlands, the Pleistocene and Pliocene of the United States (Florida), and the Pleistocene and early Miocene of Japan. Six drill holes attributed to octopods were found in epifaunal and semiburrowing crabs; three drill holes attributed to gastropods were discovered in semiburrowing and epifaunal crabs, and in a burrowing mud shrimp; and the producer of two other drill holes in epifaunal crabs is unknown. Other possible drill holes occur in decapods from the Holocene and early Miocene of Japan and the late Eocene of the United States. Drill-hole predation intensities in decapod faunas by stratigraphic formation are low (#2.7%), at least in part due to multiple biases such as preservation and molting.

Impacts of bioturbation on temporal variation in bacterial and archaeal nitrogen-cycling gene abundance in coastal sediments.

In marine environments, macrofauna living in or on the sediment surface may alter the structure, diversity and function of benthic microbial communities. In particular, microbial nitrogen (N)-cycling processes may be enhanced by the activity of large bioturbating organisms. Here, we study the effect of the burrowing mud shrimp Upogebia deltaura upon temporal variation in the abundance of genes representing key N-cycling functional guilds. The abundance of bacterial genes representing different N-cycling guilds displayed different temporal patterns in burrow sediments in comparison with surface sediments, suggesting that the burrow provides a unique environment where bacterial gene abundances are influenced directly by macrofaunal activity. In contrast, the abundances of archaeal ammonia oxidizers varied temporally but were not affected by bioturbation, indicating differential responses between bacterial and archaeal ammonia oxidizers to environmental physicochemical controls. This study highlights the importance of bioturbation as a control over the temporal variation in nitrogen-cycling microbial community dynamics within coastal sediments.

Ecological periodic tables for benthic macrofaunal usage of estuarine habitats: Insights from a case study in Tillamook Bay, Oregon, USA

This study validates the ecological relevance of estuarine habitat types to the benthic macrofaunal community and, together with previous similar studies, suggests they can serve as elements in ecological periodic tables of benthic macrofaunal usage in the bioregion. We compared benthic macrofaunal Bray–Curtis similarity and the means of eight benthic macrofaunal community measures across seven habitat types in Tillamook Bay, Oregon, USA: intertidal eelgrass (Zostera marina), dwarf eelgrass (Zostera japonica), oyster (Crassostrea gigas) ground culture, burrowing mud shrimp (Upogebia pugettensis), burrowing ghost shrimp (Neotrypaea californiensis), sand and subtidal. Benthic macrofaunal Bray–Curtis similarity differed among all the habitats except ghost shrimp and sand. The habitat rank order on mean benthic macrofaunal species richness, abundance and biomass was dwarf eelgrass ≈ oyster ≥ mud shrimp ≈ eelgrass > sand ≈ ghost shrimp ≈ subtidal. The benthic macrofaunal habitat usage pattern in Tillamook Bay was, with a few exceptions, similar to that in two other US Pacific Northwest estuaries. The exceptions indicate variants of eelgrass and ghost shrimp habitat that differ in benthic macrofaunal usage perhaps due to differences in the coarseness of the sand fraction of the sediments in which they live. The similarities indicate periodic benthic macrofaunal usage patterns across the other habitat types extend over a wider geographic scale and range of environmental conditions than previously known.

Physiological consequences of parasite infection in the burrowing mud shrimp, Upogebia pugettensis, a widespread ecosystem engineer

The burrowing mud shrimp, Upogebia pugettensis, is an important ecosystem engineer throughout bays and estuaries along the Pacific coast of North America. Populations of U. pugettensis have recently declined throughout its range. A likely reason for this decline is the arrival of an invasive bopyrid isopod parasite, Orthione griffenis, which has colonised the system and increased in prevalence. We tested the following three hypotheses regarding this host–parasite system: (1) parasite infection is correlated with the volume of water processed by the host; (2) infection negatively affects host’s energetic state; and (3) infection causes feminisation in male hosts. We used several physiological and morphological measures to quantify the effects of this parasite infection on U. pugettensis. The parasite appears to have different physiological effects on male and female hosts. Our study provides mixed support for the previous theory that predicted the mechanistic interactions between this host and its new parasite. Recent examples from other systems have demonstrated that invasive parasites can have far-reaching influences when they infect ecosystem engineers. Given the negative effects of O. griffenis on U. pugettensis, this invasive parasite may have similarly large impacts on Pacific North-west estuaries throughout its invaded range.

Ecological periodic tables for benthic macrofaunal usage of estuarine habitats in the US Pacific Northwest

This study shows that spatially and temporally recurring benthic macrofauna–habitat patterns validate the ecological relevance of habitat types to benthic macrofauna and suggest they can serve as elements in ecological periodic tables of benthic macrofaunal usage. We discovered patterns across nine habitat types (intertidal eelgrass [ Zostera marina], dwarf eelgrass [ Zostera japonica], oyster [ Crassostrea gigas] ground culture, burrowing mud shrimp [ Upogebia pugettensis], burrowing ghost shrimp [ Neotrypaea californiensis], shell, sand, mud, and subtidal) on a variety of benthic macrofaunal community state variables in Grays Harbor, Washington, USA and compared them to those in Willapa Bay, Washington, USA. There were nominal differences in benthic macrofaunal Bray–Curtis similarity between all the habitats investigated except eelgrass and oyster in both estuaries. Across-habitat patterns on mean benthic macrofaunal species richness, abundance, biomass, abundance of deposit, suspension and facultative feeders, a dominance and a diversity index for the five habitats common to both studies were the same on a rank measurement scale: eelgrass ≈ oyster > mud shrimp > ghost shrimp ≈ subtidal. The patterns for most of the habitats and benthic macrofaunal measures were the same on a ratio measurement scale.

Ecological periodic tables for nekton usage of four US Pacific Northwest estuarine habitats

We compared the species composition and abundance of the total nekton community, using the Bray–Curtis similarity coefficient, and mean total nekton, fish and crab species richness, abundance and biomass, and shrimp abundance across four intertidal habitats in a US Pacific Northwest estuary: (i) eelgrass ( Zostera marina ); (ii) burrowing mud shrimp ( Upogebia pugettensis ); (iii) burrowing ghost shrimp ( Neotrypaea californiensis ); and (iv) unvegetated sand. Field sampling was conducted during daytime high tides, and was quantitative, stratified-by-habitat, randomized, and estuary-wide. More than 10 000 nekton specimens belonging to 64 taxa were collected in 454 samples during 10 sampling periods, each approximately one-month-long (from June to November), over 3 years (1998–2000). Non-metric multidimensional scaling analyses revealed annually recurring across-habitat patterns in total nekton Bray–Curtis similarity. Two-way (habitat, year) analyses of variance revealed annually recurring across-habitat patterns on 10 indicators of nekton-habitat quality and preference. Total nekton species richness, abundance, and biomass were, respectively, on average, 8 ×, 25 ×, and 25× greater in eelgrass, 4 ×, 6 ×, and 5× greater in mud shrimp, and 2 ×, 3 ×, and 2× greater in ghost shrimp, than in sand habitat. Our findings validate the ecological relevance of our habitats to nekton, and suggest they can serve as elements in ecological periodic tables of nekton habitat usage.

Is the Collapse of Mud Shrimp (Upogebia pugettensis) Populations Along the Pacific Coast of North America Caused by Outbreaks of a Previously Unknown Bopyrid Isopod Parasite (Orthione griffenis)?

A dramatic increase in prevalence of the recently discovered bopyrid isopod parasite, Orthione griffenis, likely introduced in the 1980s from Asia to the Pacific coast of North America, coincided with the 2002 collapse of a population of its burrowing mud shrimp host, Upogebia pugettensis, in Willapa Bay, Washington that had been stable since monitoring began in 1988. An examination of whether O. griffenis infections were sufficient to cause this decline and other recently noted U. pugettensis population collapses in Pacific Coast estuaries was conducted. O. griffenis prevalence was the highest in large reproductive-sized female shrimp and caused an estimated average 68% loss of U. pugettensis reproduction in Yaquina Bay, Oregon over a 5-year period. O. griffenis prevalence fluctuated from year to year, but trends were similar in all estuaries sampled. Uninfected shrimp transplanted back into locations from which they had disappeared acquired the parasite, suggesting that O. griffenis is extremely effective at finding its host even in estuaries with very low host density. Since both U. pugettensis and O. griffenis have pelagic larval stages, their population dynamics are also influenced by coastal nearshore oceanography and estuarine recruitment success. Coastwide lack of estuarine recruitment appears to coincide with declines in density of a co-occurring thalassinid shrimp, Neotrypaea californiensis, but cannot alone explain U. pugettensis population collapses. Although patterns observed to date could be explained by the presence of either a native or introduced parasitic castrator, assumptions of a resilient co-evolved host–parasite relationship do not apply for introduced species, so continued efforts to follow the spatial extent and consequences of the O. griffenis–U. pugettensis host–parasite relationship are warranted.

Effects of a newly invasive parasite on the burrowing mud shrimp, a widespread ecosystem engineer

The burrowing mud shrimp Upogebia pugettensis is an important ecosystem engineer in Pacific bays and estuaries from Alaska to Baja California. Recently, mud shrimp populations throughout this range have declined precipitously. This decline has followed invasion by a bopyrid isopod, Orthione griffenis, which parasitizes and removes hemolymph from the shrimp's gill cham- bers. However, a causal link between this invasive parasite and the decline of its host has yet to be demonstrated. I used observed allometric relationships between the parasite and its host, spatial pat- terns of parasite prevalence across host demographics, and simulation modeling to explore potential mechanisms leading to this causal link. Results here, considered with other work, suggest that this parasite may hamper host reproduction by increasing metabolic demands. First, shrimp are more likely to become infected with increasing exposure to parasite-laden water, which varies both with the proportion of time that tides cover individual shrimp burrows and with each shrimp's size-specific pumping rate of water through its burrow. Second, parasites impose a metabolic burden on their host that is proportional to parasite size, which itself increases with time since infection. Third, increasing metabolic costs in turn reduce reproductive capacity, potentially through feminization of male hosts. Fourth, increased metabolic costs of infection are most detrimental when feeding time is limited, which occurs in higher intertidal areas. These conclusions should be taken as testable hypotheses that, if examined, will elucidate this host-parasite interaction and clarify if this new invasive parasite is capable of reducing and eliminating this important ecosystem engineer.

The consequences of changes in abundance of Callianassa subterranea and Amphiura filiformis on sediment erosion at the Frisian Front (south-eastern North Sea)

In the early 1990’s a conspicuous shift took place in the density of two key macrofauna species at the Frisian Front (SE North Sea). The density of the formerly dominant brittlestar Amphiura filiformis showed tenfold reduction and remained low throughout the observation period (1986–2000). In the same period, the burrowing mud shrimp Callianassa subterranea showed a fourfold increase in density. Since the Frisian Front is a transition area where tidal currents fall just below the erosion threshold of silt and bioturbating mud shrimps can potentially affect the sediment erosion threshold, we examined the effects of the species on sediment erodibility. Two experiments were conducted in laboratory annular flumes. In the first experiment we compared the effects of pre-shift and post-shift combinations of the two species on the erodibility of Frisian Front sediment. The results indicated that the erosion was facilitated by a combination of high densities of C. subterranea and low densities of A. filiformis, representing the situation in the late 1990s. The difference in erodibility was already apparent at velocities equal to the critical near-bed current speed measured at the Frisian Front. In the second experiment the effects of pre- and post-shift densities of A. filiformis on sediment erodibility were compared. This showed that low A. filiformis densities as found in the late 1990’s facilitate erosion, but the effect is only significant at velocities above the critical near-bed velocity in the field. At the latter velocity, no significant difference in erodibility was found between the two A. filiformis densities. This implies that the difference in turbidity in the first experiment was mainly due to the activity of C. subterranea. The experimental results indicate that resuspension at the Frisian Front may occur more frequently as a result of the shift towards a Callianassa dominated community. More frequent resuspension of bottom sediment, most likely amplified by the climate induced increase of wind strength in the North Sea, may hamper the recovery of the A. filiformis adult population.

GILL-CLEANING MECHANISMS OF THE BURROWING MUD SHRIMP LAOMEDIA ASTACINA (DECAPODA, THALASSINIDEA, LAOMEDIIDAE)

Gill-cleaning mechanisms of the burrowing mud shrimp Laomedia astacina De Haan, 1849, were examined based on morphology and behavioral observations. The gill complement consists of 13 arthrobranchs and 5 podobranchs, with flattened gill filaments of the phylloid trichobranch type. Gill cleaning is based on passive mechanisms involving setal systems on the scaphognathite, epipods, setobranch, and pereiopodal coxae. Multidenticulate scaphognathite setae (MSS) bearing digitate scale setules project into the gill chamber, lying over gill filaments. Proximal setules of the MSS incline to the setal base while distal setules incline to the tip; the transition zone of setule inclination is marked with an annulus. Setiferous epipods on the limb bases, except on fifth pereiopods, are armed with serrate setae, which contact adjacent gill filaments and coxal surfaces. Multidenticulate setobranch setae are found only on the coxae of third maxillipeds, thus limiting their gill cleaning functions to the anterior gills. Pereiopodal coxae bear tufts of short serrate setae together with a few multiple double-prong setae that are morphologically atypical in decapods. Active gill cleaning by pereiopodal brushes, as in callianassids and upogebiids, and limb rocking, as in astacideans, were not observed. Among thalassinideans, gill-cleaning mechanisms of laomediids appear more closely allied to those of thalassinids than callianassids and upogebiids, whereas those of axioids possibly indicate an ancestral condition.

Naushonia Lactoalbida, New Species (Decapoda: Thalassinidea: Laomediidae), a Mud Shrimp from Inhaca Island, Moçambique

A new species of the rare burrowing mud shrimp genus Naushonia has been found at Inhaca Island, in southern Mozambique. This is the sixth species in the genus, the first one found in the southern hemisphere and the second one found in the Indian Ocean. It was obtained from the entrance of its burrow in low water on a tidal flat. The species of the genus Naushonia have a confusing systematic history. Perhaps be­ cause of the subchelate first pereiopods and simple second pereiopods, de Man (1920) incorporated Naushonia crangonoides Kingsley, 1897, and Coralliocrangon perrieri Nobili, 1904, in the Crangonidae. Al­ though the linea thalassinica was pointed out as a similarity between the two genera, no comments were made about the trans­ verse suture of the uropods, which was used in the description of the family Laomediidae (see de Man, 1928). The reptant ap­ pearance with stiff antennae, a short and broad rostrum, and an unfortunate loss of all pereiopods caused Rathbun (1901) to erect a new genus, Homoriscus, for the new species H. portoricensis . Using branchial structure and the above mentioned criteria, Chace (1939) synonymized these genera with Naushonia, in the subfamily Naushoniinae, family Laomediidae. The genus seems to be rare, and very few findings of specimens be­ longing to these species have been reported. Four of the five species in this genus are found on American coastlines: A^. crango­ noides, east coast of the U.S.A. (Kingsley, 1897); N. portoricensis (Rathbun, 1901) Caribbean Sea (Rathbun, 1901); N. macginitiei (Glassell, 1938) Mexico and Cali­ fornia (Glassell, 1938); A^. panamensis Martin and Abele, 1982 Pacific coast of Panama (Martin and Abele, 1982). The fifth, N. perrieri, is known from the Red Sea and Somalia coast line (Nobili, 1904). The pres­ ent finding is the first from the southern hemisphere and the second from the Indian Ocean.

NAUSHONIA LACTOALBIDA, NEW SPECIES (DECAPODA: THALASSINIDEA: LAOMEDIIDAE), A MUD SHRIMP FROM INHACA ISLAND, MOÇAMBIQUE

A new species of the rare burrowing mud shrimp genus Naushonia has been found at Inhaca Island, in southern Mozambique. This is the sixth species in the genus, the first one found in the southern hemisphere and the second one found in the Indian Ocean. It was obtained from the entrance of its burrow in low water on a tidal flat. The species of the genus Naushonia have a confusing systematic history. Perhaps be­ cause of the subchelate first pereiopods and simple second pereiopods, de Man (1920) incorporated Naushonia crangonoides Kingsley, 1897, and Coralliocrangon perrieri Nobili, 1904, in the Crangonidae. Al­ though the "linea thalassinica" was pointed out as a similarity between the two genera, no comments were made about the trans­ verse suture of the uropods, which was used in the description of the family Laomediidae (see de Man, 1928). The reptant ap­ pearance with stiff antennae, a short and broad rostrum, and an unfortunate loss of all pereiopods caused Rathbun (1901) to erect a new genus, Homoriscus, for the new species H. portoricensis . Using branchial structure and the above mentioned criteria, Chace (1939) synonymized these genera with Naushonia, in the subfamily Naushoniinae, family Laomediidae. The genus seems to be rare, and very few findings of specimens be­ longing to these species have been reported. Four of the five species in this genus are found on American coastlines: A^. crango­ noides, east coast of the U.S.A. (Kingsley, 1897); N. portoricensis (Rathbun, 1901) Caribbean Sea (Rathbun, 1901); N. macginitiei (Glassell, 1938) Mexico and Cali­ fornia (Glassell, 1938); A^. panamensis Martin and Abele, 1982 Pacific coast of Panama (Martin and Abele, 1982). The fifth, N. perrieri, is known from the Red Sea and Somalia coast line (Nobili, 1904). The pres­ ent finding is the first from the southern hemisphere and the second from the Indian Ocean.

Effects of a burrowing mud shrimp, Upogebia pugettensis (Dana), on abundances of macro-infauna

Burrowing ghost shrimp (Callianassidae) have been shown to exert a strong influence on the abundance of macro-infauna in soft-sediment communities, especially through reduction in the densities of many sedentary species. However, relatively little is known about the community effects of other burrowing shrimp, such as mud shrimp, Upogebia spp., that occur commonly in many estuaries of North America. A transplant/exclusion experiment was conducted to examine the effects of Upogebia pugettensis (Dana) on the abundance of other macro-infauna in a Pacific Northwest tideflat. Several numerically dominant, sedentary crustaceans and polychaetes exhibited lower abundances in the presence of Upogebia as compared to treatments where the mud shrimp was absent. The overall pattern of faunal response to the presence of U. pugettensis was similar to that reported for Callianassa californiensis (Dana), an unexpected finding given the different burrowing and feeding habits of these two crustaceans.

Zoeal Stages of the Burrowing Mud Shrimp Laomedia astacina DE HAAN (Decapoda: Thalassinidea: Laomediidae) Reared in the Laboratory

Zoeal Stages of the Burrowing Mud Shrimp Laomedia astacina DE HAAN (Decapoda: Thalassinidea: Laomediidae) Reared in the Laboratory