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Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, California 95039-9644
* To whom correspondence should be addressed. E-mail: jdrazen{at}mbari.org
Localized areas of intense biological activity, or hot spots, in the deep sea are infrequent but important features in an otherwise sparsely occupied habitat (1). Hydrothermal vents, methane cold seeps, and the tops of seamounts are well documented areas where dense communities persist for generations (2–5). Reproductive aggregations where conspecifics concentrate for the purposes of spawning or egg brooding could be thought of as transient hot spots. It is likely that they occur in populations with low densities to maximize mate location and increase reproductive success (6). However, only a few deep-sea reproductive aggregations have ever been documented (7–9), demonstrating the paucity of present-day information regarding reproductive behavior of deep-sea animals. In this paper we describe a unique multispecies reproductive aggregation located on the Gorda Escarpment, California. We document some of the highest fish and octopus densities ever reported in the deep sea, with most individuals of both species brooding eggs. We describe the nesting behavior of the blob sculpin, Psychrolutes phrictus, and the egg-brooding behavior of an octopus, Graneledone sp. observed during annual dives of a remotely operated vehicle (ROV) on the Gorda Escarpment. The animals are concentrated at the crest of the local topography and near cold seeps where they may benefit from enhanced current flow and local productivity. These findings provide new information on the reproductive behaviors of deep-sea animals. More importantly, they highlight how physical and bathymetric heterogeneity in the environment can result in reproductive hot spots, which may be a critical resource for reproductive success in some deep-sea species.
Fifteen ROV dives were conducted on the Gorda Escarpment and Mendocino Ridge during three visits in August 2000, August 2001, and July 2002 (Fig. 1). The Gorda Escarpment is a submarine plateau offshore of northern California. The Mendocino Ridge extends westward from its northern edge at 40.35° N. The Escarpment’s northern side is characterized by steep topography, frequent rocky outcrops and talus fields, sediment slumps, and drainage channels (10). The depth of investigation ranged from 1300 to 3000 m.
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0.1–0.2 °C) due to local subsurface fluid seepage from the substrate (10). Blob sculpin attended nests of large (4.0 ± 0.6 mm; n = 50) pinkish eggs (Fig. 3A). The majority of the nests had fish in close attendance (within 3 m), often sitting directly on or touching the eggs. Some nests and fish were observed by themselves primarily in the roughest terrain where it was difficult to see behind nearby rocks and ledges. Eggs were free of sediment, suggesting that the adults cleaned or fanned their nest sites. Brooding fish were almost always found very close to each other, and nests were often on neighboring boulders separated by only 1–2 m. Generally the parent fish did not move when the ROV approached; however, this was also true for fish without eggs, which precluded any conclusions about nest-guarding behavior. The sex of the fish could not be determined from video observations. Fecundity was estimated for four egg masses and ranged from 9375 to 108,125 eggs. The eggs were generally laid on the flat exposed surfaces of large boulders and rock outcrops. Of the 64 egg masses, 57 (89%) had been laid on single rocks; the other seven were each strewn across as many as three neighboring rocks or across large fissures in a flat rock face.
This study presents the first direct evidence of parental care (11) in an oviparous deep-sea fish. It is likely that members of the families Zoarcidae and Liparidae also exhibit parental care, but this has not been confirmed. The zoarcid Melanostigma atlanticum was captured in a burrow with its eggs by a box core at 350 m depth (12). The developmental stage of the eggs was not determined; thus, it is unknown whether the parents were in the process of egg laying (one female still retained her eggs) or whether they were staying to guard and ventilate the eggs. Many liparids have large eggs and very low fecundities, suggesting some form of parental care, but no direct evidence has been described (13). Reviews of reproduction in other diverse deep-sea fishes make no note of parental care (1, 14–16).
Individuals of Graneledone sp. were observed brooding eggs under their bodies while sitting vertical and motionless with arms curled outwards on boulders, rock outcrops, and ledges (Fig. 3C). An adult specimen of Graneledone boreopacifica was collected in July 2002 with 51 eggs. The eggs were 40 mm in length, and many began hatching prematurely when collected; these juveniles still retained egg sacs. Site 1 was revisited in July 2002, and 63 individuals of Graneledone sp. were observed in the curled position. Nine of ten individuals in this position were confirmed to be in the process of brooding eggs. In August 2001, 43 eggs of a specimen of Benthoctopus sp. were collected from Site 2. This octopus, unlike the others observed, was underneath a small rock with its eggs out of plain view; it was also much smaller than the Graneledone sp. (mantle length 10 cm), and its eggs were only 16 mm long. It was only observed during the course of collecting the rock for geologic examination.
Our observations provide the first evidence of a multispecies reproductive aggregation in the deep sea. To our knowledge, the only other reproductive aggregations described from deep-sea environments are for spawning aggregations of orange roughy (7); another brooding aggregation of octopuses, including a species of Graneledone, in the North Pacific (8); and small (2–6 individuals) aggregations of an echinoid (9). In addition, there are reports of aggregations of two echinoderm species in the North Atlantic (17, 18) that may have been for the purpose of reproduction, and pair formation has been documented in a holothuroid (19). Observations over 3 years indicate that the aggregation at Site 1 is either long-lived or recurs at the same location perhaps every year. The aggregations of blob sculpin and octopus exhibit densities and biomass among the highest recorded in the deep sea (Fig. 2). Localized aggregations of this magnitude could have profound influences on local food webs and fauna.
There are several possible explanations for the presence of the dense aggregations of animals on the Gorda Escarpment. For instance, the presence of brooding aggregations of Benthoctopus sp. and Graneledone sp. in the North Pacific have been explained previously by the availability of both rocky substrate for egg attachment and bivalve prey from nearby cold seeps (8). Rocky substrate for egg attachment is an obvious requisite for spawning by both sculpin and octopus. Rocky substrate, however, occurred at all dive locations yet reproductive aggregations were present at only two locations, suggesting that substrate is not the only criterion involved in site selection for brooding. Furthermore, aggregations of sculpin or octopuses have not been observed on other rocky features, including some within our dive areas on the Gorda Escarpment and Mendocino Ridge and on the Davidson, Guide, and Gumdrop seamounts in the North Pacific. These seamounts have been observed using the Monterey Bay Aquarium Research Institute’s ROV at various times of the year, but no aggregations such as we describe have been found (J. Drazen, unpubl. data). Likewise, on more than 200 dives in the Monterey Bay area at depths greater than 1000 m and often in areas of rocky substrate (i.e., canyon walls and slopes), no brooding octopuses were observed (although octopuses are common) and only 13 blob sculpin were seen, none with eggs.
The presence of cold seeps can dramatically influence the local productivity of surrounding deep-sea communities by transfer of organic nutrients (2). Diffuse cold seeps were observed at both sites of sculpin and octopus aggregations, suggesting that enhanced local productivity from cold seeps on the Gorda Escarpment may also influence the aggregations. This is unconfirmed, however, because only six octopus were seen in the immediate vicinity of seep organisms and the distribution of nesting blob sculpin was much broader than that of the seeps (Fig. 4).
Cold seeps are related to the upward flow of warm, methane-rich pore fluids from depth; this flow has also generated slight increases in temperature (0.1–0.2 °C above ambient) at Site 1 (10). Increases in temperature could shorten egg development times, which would be an advantage to species that invest parental care. Assuming a Q10 of 2, an increase of 1.5 °C would be required for a 10% reduction in incubation time. Similar conclusions were drawn for benthic octopus brooding near cold seeps at the Baby Bare site off of Washington State (8). However, temperature elevations of this magnitude around cold seeps are very unlikely. Furthermore, animal occurrences did not correlate with the highest temperature anomalies. Therefore, we conclude that cold seeps do not benefit these animals physically, but they may provide a food source that could play a role in the location of the animal aggregations.
In addition, elevated currents may influence site selection by brooding aggregations. All blob sculpin and most octopus were observed near the ridge crest where exposure to elevated currents is likely (1, 3, 20). As on seamount crests, abundant suspension feeders such as brisingid sea stars, tunicates, gorgonians, and venus flytrap anemones were found at the crest of the Gorda Escarpment, providing evidence of accelerated current speeds. Some shallow-living sculpins have a strong preference for nesting sites that are exposed to the current; this exposure aids in gas exchange and waste removal and accelerates embryogenesis (21, 22). At Site 1, where oxygen concentrations are very low, enhanced water movement may be required to deliver adequate oxygen for embryogenesis. A reduction in the need to ventilate or fan the eggs could be an energetic benefit to the adults. In addition, benthic egg brooding and hatching implies a demersal larval/juvenile phase (23). Bottom currents in the deep sea are generally low, so these organisms may take advantage of intensified currents at this site to enhance the dispersal of larvae or juveniles within the demersal habitat.
At one time the deep sea was thought to be a sparsely populated and homogenous environment (1). Today, dense localized communities such as the chemosynthetic communities of hydrothermal vents and methane cold seeps (2) and the suspension-feeding communities of seamounts (3) are well known. Our study site on the Gorda Escarpment is another unique type of biological hot spot in the deep sea. The site is connected to the continental margin but topographically exhibits characteristics of a seamount environment. In addition, small cold seeps are present. We hypothesize that the local topography interacting with the physical and geologic setting has created a localized reproductive hot spot in the deep sea utilized by at least two very different animals.
This information has several important implications. The reproductive hot spot on the Gorda Escarpment (and future sites determined to be similar) might qualify as an area to be protected from fishing. The protection of habitats associated with vulnerable life stages, notably spawning aggregations, is a main objective of marine reserves (24). Our study site could be threatened by commercial trawling and long-lining operations. In the last two decades, the world has seen a rapid development of deep-sea fisheries to depths of 2000 m, and currently fishers regularly operate at depths of 1000 m off of the west coast of the United States (25). From an ecological perspective, our findings contribute to our understanding of habitat heterogeneity within the broader deep-sea ecosystem as well as providing sites where scientists can predictably observe reproductive biology in deep-sea animals, a prospect that is exciting for the study of these elusive species.
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  J. Sellanes, E. Quiroga, and C. Neira Megafauna community structure and trophic relationships at the recently discovered Concepcion Methane Seep Area, Chile, ~36{degrees}S ICES J. Mar. Sci., June 19, 2008; (2008) fsn099v1. [Abstract] [Full Text] [PDF]
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