Tadpole shrimp, Triops longicaudatus (LeConte), are a species of temporary, freshwater habitats. Tadpole shrimp are pests of rice production systems in California and have recently been found impacting Missouri rice fields and present in northeastern Arkansas rice fields. These impacts take the form of stand reduction by direct feeding on seedlings and uprooting seedlings during foraging. In addition, their foraging behavior causes water to become muddy, which reduces light penetration to submerged seedlings and consequently delays the development of the rice plant. Once rice is past the seedling stage, tadpole shrimp may be beneficial. This article provides information on the life cycle of tadpole shrimp, describes a new method for scouting for tadpole shrimp in rice fields, and provides scouting results and management implications.
integrated pest management
Tadpole shrimp, Triops longicaudatus (LeConte) (Branchiopoda: Notostraca: Triopsidae) (Fig. 1), are a species of temporary, freshwater habitats (Longhurst 1955). Puddles and temporary pools are ideal environments for tadpole shrimp. When considering production of rice, a rice field is flooded and drained, sometimes several times in a season, which mimics the environment of a temporary pond. Therefore, a rice field is an ideal environment for tadpole shrimp because they are pests of water-seeded rice production systems in California (Godfrey and Espino 2009) and recently were found in rice fields in the midsouthern United States (Tindall et al. 2009). This article provides information on the life cycle of the tadpole shrimp, describes a new method of scouting for tadpole shrimp in rice fields, and provides scouting results and management implications.
Tadpole shrimp display large amounts of morphological variation and exist in populations that may or may not contain males (Sassaman et al. 1997). Although eggs may not have to have a period desiccation (Scott and Grigarick 1979), other research shows that eggs need a period or multiple periods of drying before hatching (Fry and Mulla 1992). The length of time that eggs are viable is not known but eggs are viable for at least 34 mo (Scott and Grigarick 1979). If their behavior is similar to a related species, the brine shrimp, Artemia franciscana Kellogg, tadpole shrimp eggs may survive substantially longer because brine shrimp eggs were found to be viable after 10,000 yr, but this is an exceptional length of time for a resting state (Browne 1993). Immature tadpole shrimp do not all hatch from desiccated eggs at the same time when exposed to water; rather, the eggs laid by a single female hatch over several floodings (Hildrew 1985, Brendonck and Persoone 1993, Simovich and Hathaway 1997).
Females have two brood pouches on the 11th segment and can carry as many as 68 eggs per pouch. She will carry the eggs anywhere from 19 h to several days (Scott and Grigarick 1978) before she lays them on decaying or living plant material, algae, or in the soil (Takahashi 1977a). Tadpole shrimp females lay an average of 81 eggs in 24 h (Scott and Grigarick 1978) but as many as 246 eggs can be laid in 1 d by an individual (Takahashi 1977a). A female is able to lay eggs throughout her life after she reaches sexually maturity, although as she ages, eggs become misshapen (Scott and Grigarick 1978).
Several factors affect the hatching of eggs, which hatch at water temperatures >61°F, but optimal hatch occurs when water temperature is 63–75°F (Scott and Grigarick 1979). Eggs do not hatch in water that is 84°F or warmer. When exposed to saline water at a concentration of 999 ppm, eggs are able to hatch, but not at concentrations of 2,996 ppm; however, when eggs were removed from the high saline concentration and exposed to freshwater, eggs hatched (Horne 1967). Although eggs hatch when the pH of water is 3.1–10.1, the optimal pH for egg hatch is 5.6 (Scott and Grigarick 1979). The depth of flood does not appear to affect the propensity of an egg to hatch. However, the depth at which eggs are buried in the soil affects their propensity to hatch; as little as 1.27 cm (0.5 in.) of soil over them can prevent eggs from hatching (Scott and Grigarick 1979). Eggs also require dissolved oxygen present in the water to hatch (Scott and Grigarick 1979).
Given the appropriate conditions, eggs will hatch within 24 h after being exposed to water (Takahashi 1977a; Scott and Grigarick 1978, 1979). After hatching, the tadpole shrimp will grow and, like other arthropods, will molt. After their first molt, they resemble the adult. Eventually, they will molt 10–15 times before becoming adults and are sexually reproductive (Scott and Grigarick 1978). A tadpole shrimp bears a resemblance to tadpoles and possesses a mud-colored, shovel-shaped shield over the front portion of its body and two long tails originating from the last segment. They are ≈1.52 cm (0.6 in.) when they reach sexual maturity and will continue to molt after reaching adulthood until they reach their full size of 3.8 cm (1.5 in.) (Godfrey and Espino 2009).
Some of the factors that affect egg hatch also influence immature and adult tadpole shrimp development. The optimal development of tadpole shrimp occurs at 77–86°F (Scott and Grigarick 1979). Although individuals reared at 86°F were smaller than those reared at lower temperature, they reached sexual maturity at an earlier age (Fry-O'Brien and Mulla 1996). The optimal pH for immature tadpole shrimp survival is 5.7–5.9 (Hamasaki and Ohbayashi 2000). Sexually mature tadpole shrimp occur as early as 8–10 d after eggs are exposed to water (Takahashi 1977a, Scott and Grigarick 1978) and are ≈1.52 cm (0.6 in.) or larger (Godfrey and Espino 2009). Because tadpole shrimp have hemoglobin in their blood, they are able to survive in water with a low concentration of dissolved oxygen (Horne 1971). The average lifespan of tadpole shrimp after hatching from the egg is 32 d, but they can live as long as 49 d in the laboratory (Scott and Grigarick 1978).
Young tadpole shrimp feed on diatoms and protozoa in the mud (Longhurst 1955). Older instars have feeding behaviors similar to that of the adults, which consume vegetative material and aquatic invertebrates (Walton et al. 1990). They are also cannibalistic (Scott and Grigarick 1978).
Damage to Rice.
To understand how and when tadpole shrimp are a pest of rice, one must understand the different planting methodologies used in rice production in the United States. Farmers either dry-seed or water-seed their fields when planting rice. Dry-seeding involves drill-seeding or dry-broadcasting seed in dry soil. The field may be flushed (an intermittent shallow flood followed by drainage) several times to allow rice to germinate and grow in absence of rainfall but before applying a flood. A flood is established typically around the 4–5 leaf stage so that plants are not completely submerged at the time of flooding (Blanche et al. 2009). Water-seeding involves planting pregerminated or dry seeds by air into a flooded field. There are three strategies for establishing floods in water-seeded rice: delayed flood, pinpoint flood, and continuous flood. In a delayed flood system, water is drained from the field shortly after planting and the field is flushed periodically (if needed) until the establishment of the flood, which occurs several weeks after rice emerges through the soil. When the field is flooded, plants are not typically completely submerged. In a pinpoint flood system, the field is briefly drained so that roots can anchor into the soil. The field is usually without water for 3–5 d before the flood is applied and seedlings are submerged. In a continuous flood system, the flood is not drained until rice is mature before harvest (Blanche et al. 2009).
Water-seeded rice planted with pinpoint or continuous floods is vulnerable to damage by tadpole shrimp because the submerged, small seedlings do not have root systems strong enough to tolerate their foraging behavior. Once rice plants break the surface of the flood, plants are considered to be safe from injury by tadpole shrimp (Godfrey and Espino 2009). Tadpole shrimp hatch within 24 h after eggs come in contact with water (Takahashi 1977a; Scott and Grigarick 1978, 1979); therefore, tadpole shrimp hatch soon after the field is flooded. They begin to grow, feeding on microorganisms in the soil. These young tadpole shrimp do not damage rice, but after the first several molts, they adopt the feeding habits of the adults, and will feed directly on the seeds and young seedlings (Scott and Grigarick 1978). In addition, they will forage on the soil surface where their shovel-shaped heads stir the soil and uproot the small seedlings (Fig. 3) This activity muddies the water, which reduces penetration of light to submerged seedlings (Fig. 4) (Godfrey and Espino 2009). Uprooting seedlings reduce stand, which can reduce yield, and muddy water reduces photosynthesis and delays maturity. Because tadpole shrimp can reach full size within 8–10 d (Takahashi 1977a, Scott and Grigarick 1978), rice plants have <8 d to break the surface of the flood.
The uprooting of rice seedlings is characteristic of tadpole shrimp damage resulting from foraging activities. Photographic Credit: Jack Kelly Clark, courtesy University of California Statewide IPM Program.
Muddy water caused by shrimp foraging activities which reduces light penetration causing reduced growth rate of submerged plants.
The issue of stand loss can be greater depending on the variety of rice planted and the seeding rate. Hybrid rice varieties are planted at a lower seeding rate (20–30 lbs/A for delayed floods) than conventional varieties (70–110 lbs/A for delayed floods). For continuous and pinpoint flood systems, seeding rates are typically higher. Low seeding rates makes stand loss more critical than at high seeding rates. Therefore, varieties, like hybrids, are more susceptible to stand loss because of tadpole shrimp than varieties planting at higher seeding rates. For example, losing 10% of a stand planted at 30 lbs/A is more detrimental than losing 10% of a stand planted at 90 lbs/A.
Because tadpole shrimp do not hatch from eggs until exposed to water, rice that is grown in dry-seeded systems and not flooded until rice is at the 4–5 leaf stage should be safe from tadpole shrimp injury. This practice promotes large plants with adequate root systems when the field is flooded. However, heavy rainfall or flooding shortly after seeding can cause drill seeded rice to mimic a water-seeded rice production system if the field is not able to be drained; this situation can lead to tadpole shrimp damaging rice in a dry-seeded system.
The number one control option for tadpole shrimp is to avoid water-seeding rice and to flood a field after the rice has an established root system. However, in fields that are water-seeded, the field should be seeded as soon as possible after the flood is established because tadpole shrimp hatch once a field is flooded. This will minimize the amount of time that tadpole shrimp grow and maximize the growth of rice plants while tadpole shrimp are still small. The idea is that the rice will grow out of the vulnerable stage before tadpole shrimp can damage the rice.
Draining a field can be useful in killing tadpole shrimp, but rainfall can prevent this from being effective (Godfrey and Espino 2009). However, greater input costs (i.e., additional applications of herbicide, fertilizer, or both; pumping costs; and other expenses) are associated with draining (Hesler et al. 1992, Quisenberry et al. 1992, Thompson et al. 1994). From a pesticide standpoint, pyrethroids are effective at killing tadpole shrimp (Walton et al. 1990, Mulla et al. 1992); however, tadpole shrimp are not on the label but may be controlled when targeting other early season insect pests of rice. Godfrey and Espino (2009) provide treatment information for California rice production, but products labeled vary by state. Therefore, it is important in to consult your local University extension office for products available in your area.
Because animals can spread eggs (Green and Figuerola 2005), it is likely that eggs can be transported from an infested field to a noninfested field on the soles of boots of workers or on agricultural equipment when moving between fields.
Beneficial Characteristics of Tadpole Shrimp.
Tadpole shrimp do not damage only rice when foraging in rice fields. They are just as likely to uproot small weed seedlings as well (Takahashi 1977b, Yonekura 1979, Croel and Kneitel 2011). Therefore, if rice is past the vulnerable stage, tadpole shrimp can serve as a biological control of weeds. Tadpole shrimp have been employed in transplanted rice production systems to control weeds. Yonekura (1979) recommends infesting paddies with tadpole shrimp at a rate of 5/ft2 to be effectively control weeds. Also, they are predaceous on small insects, including aquatic stages of mosquitoes (Fry-O'Brien and Mulla 1996).
Scouting Methodology and the Missouri Distribution Survey.
In the spring of 2010, a distribution survey was undertaken to determine where this pest occurs in rice-producing areas of Missouri. After failed attempts to locate tadpole shrimp in fields during the spring with aquatic sweep nets, we modified the methods of Weeks and Marcus (1997) and sampled for desiccated resting eggs. After harvest, the top inch of soil in a (162.56-cm2) (64-in.2) area was removed with a shovel from five different locations (subsamples) within each sampled field. Low areas of the field were targeted because tadpole shrimp congregate in areas where water remains in the field after it is drained (Fig. 5). There was a distance of at least 15.24 m (50 ft) between subsamples. Subsamples were placed into individual plastic bags and transported to the laboratory where the soil was dried completely to enhance egg hatch (Fry and Mulla 1992). Drying was accomplished by opening the plastic bags and exposing the collected soil to air for up to 2 wk under greenhouse bench conditions.
Tadpole shrimp congregated in a low area after drainage of the field.
After drying, the soil from each subsample was placed in its own plastic container, sized such that soil depth would be no >1.27 cm (0.5 in). Tap water was poured into a large container and allowed to come to room temperature because the temperature of water can impact egg hatch. Once at room temperature, water was added as needed to the containers of soil to maintain a 5.8-cm (2-in) flood for 15–21 d. The containers were kept in a greenhouse in Portageville, MO by using natural light (winter to spring day lengths) at 75°F. However, tadpole shrimp are hatched easily under household conditions (Halliday 2008). Given that tadpole shrimp can complete their life cycle on average in 32 d (Scott and Grigarick 1979), the containers should be examined for tadpole shrimp 2 and 3 wk after adding water. A bright light or small fish net will aid in the detection of the tadpole shrimp. In addition, the water typically appears muddy, indicating tadpole shrimp presence as well (Croel and Kneitel 2011) (Fig. 6). When examining samples, many arthropods other than tadpole shrimp are recovered, so it is important to wait at least 2 wk before examining samples to ensure proper identification. The longer tadpole shrimp develop, the more likely that they will be identified correctly. Longhurst (1955) is a useful reference for identifying the Notostraca.
The presence of muddy water in flooded subsample containers indicates presence of tadpole shrimp.
Using the methodology described above, tadpole shrimp were detected in nine of 42 fields (Fig. 7) and all tadpole shrimp positive fields were associated with the Little River drainage system. Seven of the nine positive fields had more than one subsample with tadpole shrimp present. If a field was found positive for tadpole shrimp, the total number collected was usually <15 per field and tadpole shrimp were not recovered from every subsample. From one field, tadpole shrimp were recovered from every subsample, for 71 in total collected from this field.
Distribution of rice fields scouted for tadpole shrimp in southeastern Missouri post-2010 rice harvest.
Although this methodology was found to be effective for determining the distribution of tadpole shrimp, current data are not sufficient to determine economic thresholds, detection thresholds, or both. However, the authors feel that a heavily infested field, like the one field sampled that had tadpole shrimp present in all five subsamples, likely would be detected. Regardless of the numbers of tadpole shrimp found in a field, if samples test positive for tadpole shrimp, the farmer should be aware of the risk associated with water-seeding the field and should consider drill-seeding that field. If the farmer must water-seed, efforts should be made to seed the field as quickly as possible after the flood is established (Godfrey and Espino 2009) and planting low seeding rates should be avoided. In addition, the field should be watched closely to ensure stand loss does not become problematic in the field.
We thank the entomology crew at the University of Missouri for field assistance. This work was supported by a grant from the Missouri Rice Research and Merchandising Council.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, providedthe original work is properly cited.
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