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W. Eberhard, R. Achoy, M. C. Marin, and J. Ugalde.
Natural history and behavior of two species of Macrohaltica (Coleoptera: Chrysomelidae).
Psyche 100(1-2):93-119, 1993.

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NATURAL HISTORY AND BEHAVIOR OF TWO SPECIES OF MACROHALTICA (COLEOPTERA: CHRYSOMELIDAE) BY W. EBERHARD"~, R. ACHOY~, M. C. MAR IN^, AND J. UGALDE~'~ The genus Macrohaltica and the allied genus Altica have approximately 30 described species in Central America and per- haps 200 or more worldwide (R. White pers. comm.). Larvae and adults often feed on onagraceous and ericaceous plants (Scherer 1969, Phillips 1977a), though other plants are also utilized (Woods 1918, Balsbaugh and Hays 1972, Phillips 1977a, Barstow and Git- tins 1973, LeSage 1990). Some species of Macrohaltica are con- sidered secondary pests of crops in Costa Rica (King and Saunders 1984). Some species are difficult to distinguish morphologically (Phillips 1977b), and both parthenogenesis and interspecific hybridization are known (Phillips 1977a, 1979). This paper describes aspects of the natural history and behavior of a pair of species in the central highlands of Costa Rica, a metal- lic blue species M. jamaicensis (hereafter M. j.), and an apparently undescribed metallic purple species (hereafter M. sp.). The beetles frequently attract attention because they aggregate, sometimes in masses of up to several thousand individuals. A second striking trait is that some aggregations include individuals of both species, and cross-specific male-female pairs are common in such aggrega- tions.
MATERIALS AND METHODS
Observations were made over a span of nine years, during which time we saw many tens of thousands of beetles in the field, and raised thousands in captivity. The behavior of beetles in four aggregations was observed in detail:
Aggregation I - both species on Ludwigia octovalvis (Ona- graceae) plants near San Antonio de Escazu, el. 1300 m, 27 ' Smithsonian Tropical Research Institute Escuela de Biologia, Universidad de Costa Rica, Ciudad Universitaria, Costa Rica Institute Nacional de Biodiversidad, Santo Domingo de Heredia, Costa Rica Manuscript received 11 January 1993.




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94 Psyche [vo~. 100
June-13 July 1983). In this and other field observations, adults of M. sp. were identified by their purple color; since Fl hybrids between the species are also purple (R. Achoy unpub. thesis), these identifications are somewhat uncertain. Nevertheless hybrid indi- viduals (distinguished by genitalic characters) are uncommon in the field (Eberhard and Ugalde in prep.); Aggregation I1 - M. j. on Cuphea sp. (Litraceae) plants near the edge of a lawn near San Vito de Java, el. 1000 m, 23-25 Jan. 1987; Aggregation I11 - M. sp. on low grass in a pasture near Mon- teverde, el. 1300 m, 14-15 Feb. 1985; and Aggregation IV - M. sp. on various plants along approximately 50 m of a roadside above San Antonio de Escazu, el. 1400 m, Feb-June, 1992. These and other sites mentioned in the text are shown in Fig. 1.
All beetles in Aggregation I were counted on 12 nights. Each night all unmarked pairs of males and females were marked on the dorsal surface with airplane enamel (two spots for males, one for females). Unmarked solitary beetles were not marked. Beetles were raised in captivity in San Jose with ambient tem- peratures and light cycles. Larvae were fed freshly cut leaves in petri dishes, and adults were fed either the same or kept in plastic bags on branches of potted food plants. When larvae ceased feed- ing and began wandering, they were placed in containers with soft soil where they could pupate.
Experiments on preferences for pupation substrates were per- formed as follows. An approximately cylindrical plastic cup (8.8 cm in diameter at the mouth) was placed in the center of an approximately cylindrical, larger plastic container (16.0 cm in diameter at the mouth). The cup was filled to the brim with one substrate and set in the center of the larger container, which was then filled to the brim of the cup with the other substrate. Larvae placed on the surface thus had access to both types of substrate (60.8 cm2 of the substrate in the cup, 140.3 cm2 of that in the larger container). Neither type of soil was compacted. After the larvae (30-40 per repetition) had disappeared underground, the smaller container was removed from the larger, and the numbers of adults reared from each were recorded. In replica experiments sub- strates in the larger and smaller containers were reversed. Voucher specimens of adult beetles are deposited in the U. S. National Museum, the British Museum (Natural History), and the



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19931
Eberhurd, Achoy, Murin & Ugalde
Pic0 Blanco
Fig. 1. Map of study area, showing sites mentioned in the text. Museo Nacional de Costa Rica housed at the Institute Nacional de Biodiversidad. Vouchers of the plants are in collections of the Mis- souri Botanical Garden, St. Louis, MO and the Escuela de Biologia of the Universidad de Costa Rica.
Unless noted otherwise, all statistical tests were two-tailed Chi squared tests. Averages are followed by one standard deviation. Altitudinal Range
The altitudinal ranges of the two species differed. The highest and lowest sites at which we found M. sp. were approximately 2300 m on Cerro de la Muerte, and about 1000 m near San Rafael de Escazu; M. j. was absent at higher elevations, occurring from



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96 Psyche [vo~. 100
San Josecito de San Isidro de Heredia and above San Antonio de Escazu (both about 1400 m) to San Rafael de Escazu (1000 m). Life Cycle
Both species were raised from egg to adult in captivity. Approx- imate durations of immature life stages were 5 days for the egg, 21 for the larva, and 14 for the pupa, but durations of the larval stage varied somewhat for both species on different host plants (Table 1). The longest adult life in captivity was 94 days for a female M. j. (a Fl hybrid female lived 99 days). Eggs were about 1.2 mm long, oval in shape, and yellowish in color. They did not have the fecal streak found on the eggs of some Altica spp. (Woods 1917, Phillips 1977a). Each egg was covered with a highly reticulate mesh of a white, somewhat extensible, adhesive material. When the egg was dry this covering gave it a white color. When a group of 50 newly- laid eggs (<24 hr old) was tasted, they produced a burning sensa- tion similar to that of the larvae (below) but weaker. Oviposition behavior of M. j. was observed in captivity. The female made repeated brief, apparently exploratory extensions of her genitalia against the substrate before ovipositing. The pair of coxites, which bear setae which are probably chemosensory and/or mechanosensory in function (Phillips 1978), projected rearward beyond the tip of the ovipositor with each extension. Table 1. Larval weight at maturity, and average development time for larvae raised on two different food plants. (/. = M. jamaicensis; sp. = M. sp.). Numbers in parentheses are total number of larvae weighed, and number of groups of larvae weighed. Larvae from all crosses were significantly lighter when raised on G. insig- nis (p<0.01 with Kruskal-Wallis using groups of larvae). Larvae of j. X j. cross raised on G. insignis were significantly lighter (Pc0.005 with Kruskal Wallis) than those of all other species.
Ludwigia octovalvis Gunnera insignis
- - -- - -
larval wt. development larval wt. development Cross at maturity time at maturity time
female male (mg) (days) (mg) (days)
j. X
j. 45.3å±2.2(533,8
14.3 10.610.2(3,2) 40.3
sp. X
sp. 42.3å±3.8(326,13 21.6
30.2(144,7) 34.7
j. X sp. 42.9å±2.2(131,5
17.5
36.651.9(111,5) 29.3
sp. X
j. 45.9å±2.0(64,4 16.4 34.7å±0.9(78,4
29.4




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19931 Eberhard, Achoy, Marin & Ugalde 97 Eggs were found on the leaves of all three genera of host plants. Those of M. sp. on the large G. insignis leaves, which were up to more than 1 m in diameter, were usually solitary, each alongside a vein of the leaf; in a sample of 728 eggs, there was one group of 9, 3 of 3, 20 of 2, while all the other 670 eggs were not within .5 mm of another egg (average group size = 1.05k0.37). In contrast, the eggs of M. j. were much more often grouped (av. group size = 10.9k10.9, range 1-59, n=1341) on the thinner and much smaller leaves of Ludwigia octovalvis (about 1 cm wide). Eggs of M. j. on L. octovalvis were nearly always on the underside of the leaf (70 of 74 groups). In captivity M. j. also laid eggs in tight spaces such as the crack between the top and bottom of a petri dish. Eggs of M. j. generally failed to hatch unless they were quite humid. Thus eggs laid on leaves of potted L. octovalvis plants in the lab (where neither rain nor dew wet the eggs) late in the wet season (Oct. 1991) often failed to produce larvae (only 21.9% of 2061 eggs in 54 groups hatched); at least one egg hatched in only 16 of 54 groups laid by 5 females (branches with eggs were enclosed in small plastic sandwich bags with many small holes). In the early dry season (Nov. 1991) hatching success was even lower (16 of 128 groups laid by 12 females, p<0.01). In contrast, when leaves on which eggs had recently been laid were placed on filter paper or paper napkins saturated with water in small, culture dishes, hatching success was much higher (79% of 506 eggs; 39 of 39 groups had at least one egg hatch) (p<0.001 compared with groups of eggs on leaves).
Survivorship of eggs and larvae on plants where adults were aggregated was probably reduced. Aggregations of adults some- times completely stripped G. insignis leaves and entire Cuphea and Ludwigia plants (Fig. 2), so eggs could be consumed along with the plant. We observed captive adults eating eggs laid on the walls of petri dishes. Larvae which eclosed on plants with aggregations of adults also ran the risk of not having adequate food. Females of at least M. sp. tended to oviposit on leaves where adults were not aggregated. Inspection of 16 pairs of G. insignis leaves, one with an aggregation of adults and the other the nearest relatively uneaten leaf of the same plant, showed that even though M. sp. beetles were seldom seen away from aggregations, the densities of eggs (eggs/cm2) were lower on the occupied leaves: average densi- ties were 4.28å±7.01/cm (range 0-26.4) vs. 6.71k6.96/cm2 (range



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98 Psyche [VOI. 100
Fig. 2. Adults of M. sp. on small (above) and large (below) !eaves of Gunnera imgnis.




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19931 Eberhard, Achoy, Marin & Ugalde 99 0-28.2) (in 13 of 16 pairs the density on the unoccupied leaf was higher, p<0.01).
Larvae remained on the host plant day and night. Although lar- val coloration was not aposematic (pale brownish yellow or orange with black head capsule, legs, and bristles), some larvae of both species had a strongly disagreeable taste. Recently moulted third instar larvae (mostly black in color) had little or no taste, but fully grown larvae (mostly orange in color) of M. sp. on G. insignis plants produced a delayed but powerful burning sensation. When one entire larva was tasted, the burning began about 30 sec later, and lasted for more than 15 minutes. A larva of M. j. on a L. octo- valvis plant and an adult M. sp. on a G. insignis plant had a similar, though less intense taste (larvae were identified by association with nearby monospecific aggregations of adults). First instar larvae generally began feeding in a group near eggs from which they hatched, but older larvae did not aggregate as they fed. The average number of M. j. larvae per occupied leaf on two L. octovalvis plants was 1.8 å 1.8 (N = 57 leaves with larvae). Early instar larvae of both species usually fed on only the lower layers of the leaf, leaving the upper side intact. Later instars ate entire leaves of Ludwigia spp., but usually left one (usually the upper) side of the much thicker G. insignis leaves intact. Larval damage to G. insignis leaves was thus easily distinguished from that produced by adults, as in some Altica (Woods 1917, 191 8). Larvae on Ludwigia plants which had been stripped of leaves also fed on the cuticle of stems and fruits. Although there was substan- tial variation, it appeared that M. j. larvae tended to feed on leaves lower down on L. octovalvis plants.
Larvae left host plants to search for appropriate pupation sites. In nature mature larvae of M. sp. (identified as such by heavily damaged Gunnera plants and the absence of Ludwigia or Cuphea plants nearby) were seen crawling on the ground 5 m from the nearest plant with larval feeding damage; mature M. j. larvae (identified by raising them to adults) were found to up to >1 m from the base of the nearest L. octovalvis. Active selection of pupation sites was demonstrated experimen- tally in M. j. When offered either rich humus or sandy soil, larvae tended to pupate in humus: 74 vs. 1 adults were raised in two repli- cas with sandy soil in the central portion, 57 vs. 13 in two replicas with sandy soil on the periphery (ratio of area in center: periphery



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100 Psyche [vo~. 100
= 1:2.31, p<0.001). Although their food plants generally grow in sites with waterlogged soil, larvae preferred to pupate in drier soil. When offered either humus soil with water barely standing (approximately 43% water content by weight) or drier humus soil (approximately 32% water content by weight), the larvae tended to pupate in the drier soil (78 vs. 0 adults in two replicas with the drier soil on the periphery (pc0.001).
Underground, larvae constructed small, ovoid pupation cham- bers. The depth of 62 chambers in captivity averaged 1.7k1.2 cm. The long axis of 56 of 59 chambers was more nearly vertical than horizontal. The chambers were closed on all sides, and the inner walls were relatively smooth, perhaps due to addition of a secre- tion as in Altica spp. (Woods 19 17, 19 18). The length of 1 1 cham- bers (average 1.05k0.10 cm) was substantially greater than that of the pupae in these chambers (average 0.68L0.02 cm). Of 59 pupae of M. j., 56 faced more nearly upward than hori- zontal, 3 were more nearly horizontal than upward or downward, and 0 were more nearly downward. As in Altica spp. (Woods 19 17, 1918, Barstow and Gittins 1973), pupae were covered with stiff bristles, presumably to keep the body out of contact with the walls of the chamber. The especially large bristles at the tip of the abdomen might seem designed to support the pupa's weight, but similar enlarged bristles occur in Altica bimarginata, which lies on its dorsum as a pupa (Woods 1917).
Young pupae were orange with black setae, while the legs and heads of M. j. pupae about to moult to adults were blue, and the abdomen was swollen and extended directly rearward instead of curling ventrally. The pupal cuticle ripped near the anterior end, and the adult pulled its antennae and legs free as movements of the abdomen pulled the cuticle posteriorly. After freeing itself from the cuticle, the adult beetle extended its hind wings, projecting them posteriorly and ventrally from under the clear elytra. Individ- uals in captivity (on moist paper towels) braced their middle and hind legs laterally during this stage. Presumably beetles in pupal chambers braced themselves in the upper end of the chamber, thus giving the hind wings room to expand in the lower portion of the chamber. This would explain why pupation chambers were longer than the pupae. Young adults remained underground at least briefly before emerging on the surface. Sex ratios were close to 50:50.



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19931 Eberhard, Achoy, Marin & Ugalde 101 48% of 914 M. sp. and 42% of 488 M. j. raised to adults were males.
Males did not emerge before females, as in some other chrysomelids (Waloff and Richards 1958). Adult females may emerge from pupation with more reserves than males. Thus of 27 survivors of a group of 88 adult M. j. which emerged in a container with moist earth and were kept with no food for about 7 days, 3 were males and 24 females (p<0.001 compared with overall sex ratio).
Host Plants
As in many other alticines (Jolivet 1988), both species were oligophagous. They fed on different but overlapping sets of host plants. Adult and larval M. sp. occurred on Gunnera insignis (Gun- neraceae) (approximately 50-150 aggregations of adults seen, totalling probably 10-25,000 beetles near Rio Hondura, Zurqui, Cerro de la Muerte, Tapanti, and about 40 km NNW of San Jose on the road to Puerto Viejo de Sarapiqui), but M. j. was never seen on this plant. On the other hand M. j. but not M. sp. adults were com- mon on Ludwigia hexapetala (Hook and Arn.) (Onagraceae) (more than 30 aggregations totalling probably >10,000 beetles seen at Rio Reventado, and Rio Barquero near Cartago). Adults and larvae of both species occurred at least occasionally on L. octovalvis (Jacq.) (estimated 100-200 aggregations of adults) and L. peru- viana (L.) (estimated 10-20 aggregations of adults) in and near the Universidad de Costa Rica in San Pedro de Montes de Oca, San Antonio de Escazu, Escazu, San Isidro de Heredia, and Cartago; M. j. was consistently more common than M. sp. on L. octovalvis (Table 2). Both species were also found on Cuphea sp. plants (Litraceae), but in monospecific aggregations (M. j. on C. calo- phylla Cham. and Schlechtd near Alajuelita about 5 KM E of Escazu, and on C. sp. near San Vito de Java, San Antonio de Escazu, and the Universidad de Costa Rica; M. sp. on C. sp. in Zurqui). Scattered adults of M. sp. were seen feeding on Tabachina longifolia (Melostomataceae) adjacent to large aggregations on G. insignis near Zurqui, and near San Antonio de Escazu. The four families of host plant are not closely related, but all are early secondary, weedy species. Ludwigia and Cuphea grow in humid soil, often with slowly moving or standing water, and are



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102 Psyche [vo~. 100
Table 2. Proportions of M. jamaicensis and M. sp. in mixed aggregations in the field on L. octovalvis plants (all purple individuals were classified as M. sp.; some may have been hybrids). An estimated minimum of 50-100 other aggregations of only M. j., and 10-30 mixed aggregations were also seen on this plant. (OCH = Ochomogo, just W. of Cartago; SAE = San Antonio de Escazu; SIH = San Isidro de Heredia; UCR = Universidad de Costa Rica). Date Site Proportion Total
M. sp. M. j.
30 V 84
6 1 84
1 VI 85
1 VI 85
14 VII 85
26 IX 85
23 IX 85
26 IX 84
VI-VII 83
22 I1 87
28 I11 87
30 XI1 85
1 I11 86
8 VI 85
10 VIII 85
18 1X 87
UCR
UCR
UCR
UCR
UCR
UCR
UCR
OCH
SAE
SJC
SJC
SAE
SAE
SAE
SAE
SIH
common in roadside ditches carrying effluents from houses in sub- urban and rural situations. Gunnera and Tabachina differ in being associated with well drained soils rather than swampy substrates, but grow in recently disturbed areas; Gunnera is associated with very high rainfall (Fernandez 1984).
Individual beetles can and probably sometimes do eat more than one food plant in nature. In one case, M. j. larvae (identified by association with mono-specific aggregation of adults) occurred in large numbers on plants of L. octovalvis which were nearly stripped of leaves, and in lower numbers on immediately adjacent Cuphea calophylla plants. In another case, a large aggregation of adult M. j. which was checked for several days first decimated a long row of L. octovalvis plants, then moved onto (and killed) sev- eral small Cuphea sp. plants before disbanding. Adults and larvae of M. sp. collected on G. insignis fed readily on L. hexapetala and L. octovalvis in captivity.




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19931 Eberhard, Achoy, Marin & Ugalde 103 The nearly complete absence of M. sp. on L. hexapetala (3 of 5,000-10,000 beetles), and the complete absence of M. j. on G. insignis (0 of several 10's of thousands of beetles) is probably related to the relative inability of the larvae of these species to develop on these plants (Table 3). In contrast, Fl hybrid larvae matured successfully on both of these species (Table 3). It appeared that G. insignis was more "difficult" for both beetle species as well as for hybrid larvae, as larval weight at maturity was lower for all crosses, and development times were longer (Table 1, see also oviposition rates below). Lower larval weights did not, however, generally lead to higher pupal mortality, except in the extreme case of the few small M. j. raised on G. insignis (Table 3).
Reproductive Behavior
Females in captivity began to oviposit several days after emerg- ing above ground. Feeding on living rather than recently picked leaves, and in more humid conditions lowered the number of days between first copulation and first oviposition, and raised the rate of egg production during the first days of oviposition (Table 4). Oviposition rates in the field may be lower. Of ten field- captured female M. j. placed on L. octovalvis plants, only 50% oviposited during the first 24 hours; 30% took 48-72 hours to oviposit; and 20% had still not oviposited 17 days later. Data for 12 M. sp. collected on L. octovalvis were 17% oviposited in the first 24 hours, 33% after 24-72 hours, and 50% after 3-7 days. The average numbers of eggs laid in these clutches were not high (17.2k17.0 for M. j., 10.8k8.7 for M. sp.; compare with Fig. 3). -
Table 3. Survivorship of Macrohaltica Jamaicensis, M. sp. and cross-specific hybrids raised on three different food plants. (/'. = M. jamaicensis; sp. = M. sp.) A is the proportion of larvae born which grew to mature larvae; B is the proportion of larvae born which emerged above ground as adults. --
Ludwigia hexapetala L. octovalvis G. insignis Cross N survivorship N survivorship N survivorship female male A B A B A B
-
j. X j. 808 0.54 565 0.95 0.93 804 0.04 0.00 sp. X sp. 305 0.39 177 0.75 0.71 181 0.86 0.56 j. X sp. 410 0.57 469 0.87 0.74 327 0.77 0.63 sp. X j. 109 0.58 0.50 131 0.87 0.69




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104 Psyche [vo~. 100
Table 4. Effect of conditions in early life on length of period before oviposition began in female M. jamaicensis, and on rate of egg production during the first four days of oviposition. Condition A: female kept on tender leaves of L. octovalvis plant from first day to adult life; Condition B: female kept in petri dish with moist paper towel and supplied with one newly picked leaf of L. octovalvis each day; Condition C: as in B but without moist towel. Males were combined with females, allowed a single copulation, then removed 1-2 hrs after copulation ended on the first day of mating. Similar matings were staged a day later, and, in conditions B and C, on each of the following two days. All pair-wise differences are highly sig- nificant (p<0.001) except number of days to first oviposition B vs. C, in which p<0.01) (Mann Whitney U Test).
--
Condition
- --
A B C
Age at first copulation (days) 7.5k0.5 9.0kO.O 8.4k1.7 No. of days from first copulation
to first oviposition 2.4k0.5 7.6k0.9 9.6k2.8 No. of eggs laid in first four days
of oviposition period 134.4k74.9 73.0k23.1 37.2k18.5 N (females) 12 2 1 13
Captive female M. sp. feeding on L. octovalvis laid many more eggs than those feeding on G. insignis. Average daily rates for the first 24 days of oviposition by 26 individuals on L. octovalvis was 6.32 eggslfemalelday (ranges 3.7 to 9.0 for averages for different females); the corresponding numbers for 15 individuals on G. insignis was 1.32 (range 0.45-1.80) (p<0.01 with Mann Whitney U Test comparing averages for 11 females on L. octovalvis with those for 10 on G. insignis).
Conditions early in adult life also affected male sexual behavior. Male M. j. separated from females and kept in two groups of 20-40 in gallon jars within 1-2 days after emerging and fed fresh cuttings of L. octovalvis once every 1-2 days all failed to mount and court females when they were 1-2 weeks old. In contrast, 19 of 19 males caged individually in plastic bags on living plants from their first day above ground mounted and courted females, often very assidu- ously, at the same age.
Both males and females mated repeatedly in captivity. Since females usually discard the spermatophores in which sperm is



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Eberhard, Achoy, Marin & Ugalde
Fig. 3. Changes in numbers of eggs laid vs. female age in M. jamaicensis feeding on L. hexapetala (a) and L. octovalvis (b-d). a) Eggs produced over approximately two months with continuous access to males (small numbers indicate numbers of females when they changed due to death or loss) (vertical bars are standard devia- tions). b) Eggs produced after a pair of copulations occurred before the first ovipo- sition, then the female was isolated until day 20 when she was kept with a male for 3 days (horizontal bar) before being isolated again. c) Numbers of females oviposit- ing during the experiment described in b). d) Numbers of eggs laid during the experiment described in b).
transferred a few hours after copulation (Eberhard and Kariko in prep.), it was possible to deduce the number of times a female which had been kept captive with a male had been inseminated by counting the numbers of spermatophores in her petri dish. Pairs of M. j. mated more often than did M. sp. pairs (Table 5). Interspe- cific crosses gave results typical of the males rather than females (Table 5), so the differences between species were apparently due to differences between males.
Females probably mate with many different males in the field. The beetles in many pairs seen at night in Aggregation I separated in the morning. When 34 individually marked female M. j. and an



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106 Psyche [vo~. 100
Table 5. Numbers of spermatophores found in petri dishes with different pairs of Macrohaltica beetles. Females were kept isolated from males for the first 9-10 days of their lives. Then each female was kept for 8-10 days with a given male ("first male"). After this time, the male was replaced with a male of the other species ("second male"). Crosses were the following: A - female M. j. first with male M. sp. then with male M. j.; B - female M. j. first with male M. j., then with male M. sp.; C - female M. sp. first with male M. j., then with male M. sp.; D - female M. sp. first with male M. sp., then with male M. j. All differences between first and second male are significant (~~0.05) except for D. All differences between M. j. males and M. sp. males within first male category are significant (p<0.001); the dif- ferences in second male data between A compared with B and D are significant (p<0.01), but those between D compared with B and C are not (all tests with Mann- Whitney U Test),
First male Second male
Female spermatophores/male/day spermatophores/male/day A. M.j. 2.12k0.50 (X M. j.) 0.52k0.37 (X M. sp.) B. M. j. 0.79k0.55 (X M. sp.) 1 S7k0.80 (X M. j.) C. M.sp. 0.81k0.53 (X M. sp.) 1.44k0.76 (X M. j.) D. M. sp. 1.73k0.45 (X M. j.) 1.51k0.70 (X M. sp.) N = 10 females for each cross
. . - -- -- .
equal number of males were placed in a cloth cage on a L. octo- valvis plant and checked each evening (9-12 PM), the same male was riding the female in successive evenings in 16 cases, different males rode on successive evenings in 16 cases, a male was riding on one evening but the female was alone on the next in 16 cases, and a female was alone on one evening but paired on the next in 10 cases. The longest certain pairing was 3 days (since marks were rapidly lost, some cases were uncertain). A single spermatophore represents only about 1% of the male's weight (Eberhard and Kariko in prep.), and spermatophores were apparently not especially costly for males. When males were kept without food they continued to produce substantial numbers of spermatophores. Fifteen male M. j. were kept in a separate cage for at least 14 days on a branch of a potted L. octovalvis. During this period each male participated in 0-8 matings, during which he spent 2-6 hours with a female in a petri dish with a moist paper towel, and was then returned to plant. Each male was then placed with a virgin, 7-21 day-old female in a petri dish with a moist



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19931 Eberhard, Achoy, Marin & Ugalde 107 paper towel but without food for three days. The number of sper- matophores found at the end of the first day (av. = 2.9k0.9) did not differ significantly from that at the end of the second (av. = 3.1k1.0). The number decreased slightly on the third day to an average of 2.4k0.7, which was similar to rates of spermatophore production when field-caught males were kept with females and fed freshly cut leaves (av. = 2.1k0.5 - Table 5) (p<0.024 compar- ing each male on second vs. third days of the experiment using the Mann Whitney U Test).
Females apparently needed to mate repeatedly to sustain egg production. Female M. j. kept continuously with a male showed a slow, continuous decline in the rate of oviposition over a period of about 60 days (Fig. 3a). In contrast, when 12 M. j. females which had mated twice (on the seventh and eighth days after they emerged above ground) were caged on potted L. octovalvis plants without access to further males, they ceased to oviposit in about a third of this time (after 20 days), and then resumed oviposition when allowed to mate again by being caged for three days with a male (Fig. 3b). Each female probably mated at least 5-10 times each during the second mating period (see above). The egg produc- tion by nine females was higher during the first 21 days of this sec- ond oviposition period (av. = 369k104 eggslfemale) than in the first 21 days of the first oviposition period (av. = 246+103 eggstfemale), despite the expectation that egg production would decrease with the female's age (Fig. 3a; see also Waloff and Richards 1958), (totals for 8 of the 9 females were greater in the second period - ~~0.045 with Signs Test). Reductions in egg pro- duction resulted from a combination of lower numbers of females ovipositing (Fig. 3c), and smaller clutches (Fig. 3d). The spermath- ecae of two isolated females which had ceased to oviposit had only small accumulations of sperm, in contrast to the thick helix of sperm seen in the spermathecae of females from the field (Eber- hard and Kariko in prep.), so lack of sperm may have been involved.
Defensive Behavior
Although adults of both species have enlarged hind femora, they differed from many other alticines in not making long jumps when disturbed (e.g. Furth 1988). Instead they only hopped or lurched



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108 Psyche [VOI. 100
forward when disturbed, allowing themselves to fall. They often seized a leaf or stem on the way down before reaching the ground. Larvae also reacted to disturbance by falling from the plant, and curled when they reached the substrate below. When held in the fingers, adults usually regurgitated a dark-colored fluid from the mouth and/or a clear liquid from the tip of the abdomen. Adult M. sp. were apparently distasteful to three species of lizard. Two Anolis bipuratus, three Sceloporus malachitious, and two Gerhonotus monticola were offered M. sp. beetles; in all cases the lizard seized the beetle in its mouth, then spit it out. Aggregations of Adults
Adults of both species usually occurred in aggregations which ranged up to more than 5000 individuals on a single plant or sev- eral neighboring plants. Usually there were slightly more males than females in an aggregation: in nine aggregations of M. sp. of more than 20 beetles, the ratio of malelfemale averaged 1.13k0.18 (total of 975 beetles, differ from 1:l p<0.01); in seven similar aggregations of M. j. the average ratio was 1.27k0.49 (total of 738 beetles, differ from 1:l p<0.01). This bias was probably not due to the sex ratio at birth, which was slightly skewed toward females (above). In both species most aggregations contained both feeding and mating individuals (e.g. Fig. 2). A few aggregations had mainly reproductively inactive beetles, which fed little or not at all; these will be discussed separately. Feeding Aggregations
In both species it was sometimes possible to "track" a feeding aggregation by locating heavily damaged leaves of G. insignis (M. sp) or a series of partially or completely stripped L. octovalvis plants along a ditch. Some trails of M. sp. damage included both adult damage (Fig. 2), and damage by larvae to nearby leaves. The longest such trails were >30 m in both species, and included up to 10-20 different plants.
At night the beetles in one mixed species feeding and mating aggregation (Aggregation I) were essentially motionless, appar- ently immobilized by low temperatures. Many were in pairs, with the male riding on the female's dorsum. In the morning most bee- tles remained tightly grouped until direct sunlight fell on them,



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19931 Eberhard, Achoy, Marin & Ugalde 109 then began to walk about. As the day advanced, the beetles became more active, and the aggregation less concentrated. Many male- female pairs separated, and beetles groomed, walked back and forth on the plant, and walked or flew onto nearby plants. Individu- als of M. sp. moved away from the night-time cluster more slowly than those of M. j. For example, at 8:30 AM of the morning of 30 June, 43% of the 74 more or less immobile beetles in the central cluster were M. sp; at 11 AM, 61% of the 36 remaining beetles were M. sp. (p<.05).
As the day wore on, new clumps of beetles formed, some on food plants and others on other species; clumps were nearly always in shaded sites during the earlier part of the day. Some of these aggregations dissolved as the day passed, and eventually the bee- tles accumulated on the host plant where the group would pass the next night. If the previous evening's host plant had not been con- sumed, some beetles stayed there, and the aggregation often reformed there the next evening. Sometimes the aggregation split into subgroups on different host plants on one night, then rejoined in a single group later.
The behavior of M. sp. aggregations on G. insignis leaves was different. There was usually little flight activity near aggregations even during the heat of the day. Judging by the freshness of dam- age to leaves, aggregations probably moved between plants much less often. The difference is presumably related to the much larger leaves of G. insignis (average >1 m in diameter), and perhaps to slower rates of feeding. These leaves (especially young ones) were occasionally completely stripped by adults, but more often the aggregation moved on before more than half of the leaf surface had been consumed (Fig. 2).
Some feeding aggregations apparently consisted largely of newly emerged adults, presumably in the vicinity of their pupation sites. No aggregation of this sort was studied in detail, but some aggregations of both species had few pairs and contained predomi- nantly soft-bodied individuals (recent emergence from under ground was confirmed in one M. sp. aggregation by finding that the males' genitalia were light in color). Two aggregations of mainly soft-bodied M. j. were found at sites where L. octovalvis plants had been completely stripped several weeks previously (judged by freshness of plants).




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110 Psyche [vo~. 100
Non-feeding Aggregations
Each of 15 randomly selected M. j. females in Aggregation I1 had very large fat bodies, but none had eggs more than 0.7 mm long (mature eggs are about 1.2 mm long). There was also a low frequency of pairs (males mounted on females) in this aggregation. Only 17% of 426 beetles were paired on the night the aggregation was collected, and approximate counts on 3 earlier nights gave even lower percentages; 43% of the 352 unpaired beetles in this aggregation were females.
Aggregation I11 of M. sp. was probably also reproductively inac- tive. The beetles did not feed during the three days they were observed (they were on low grass in a pasture), and few if any pairs formed at night (the beetles were piled on each other in some portions of the aggregation, making it impossible to count pairs). Similar lack of ovarian development was seen in 10 randomly selected females of M. sp. collected 22 Feb. 1992 from Aggrega- tion IV, which was also on grass, with Tabachina plants <10 m away. This aggregation was near the top of a steep ridge on the side of a mountain (Pico Blanco) (the other non-feeding aggrega- tion (111) of M. sp. was also near the top of a ridge.). Aggregation IV was observed over a longer period of time than the others. When first discovered on low grass at the edge of a road (22 Feb. 1992) it consisted of an estimated total of 1,000-2,000 M. sp. in several tightly packed clumps. When next seen (1 8 March), about 30 m from the first site (presumably the same aggregation - beetles were not marked until 20 March), an estimated 3,000-10,000 beetles were dispersed in herbacious growth along 3-4 m on the other side of the road. Observations just before sun- set and two nights later showed that the beetles remained dis- persed. A total of 300 beetles were marked along about 2 m of the roadside on 20 March, and marked beetles were seen over the next 75 days. Sightings of marked individuals occurred along approxi- mately 60 m of the roadbank. Estimated numbers of beetles ranged from 200-300 to several thousand (at last sighting on 3 June, there were an estimated 1,000-2,000 individuals). These estimated sizes of this aggregation are minima, as the thick vegetation and the pos- sibility that some beetles had moved away from the edge of the road meant many beetles could easily have been missed on any given visit. On the visit following marking (22 March), 9 of 300 beetles counted had marks. Assuming complete mixing, no loss of



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Eberhard, Achoy, Marin & Ugalde
Ill
marks, and no arrivals of unmarked beetles, this ratio gives an esti- mated total of approximately 10,000 beetles in the aggregation on 20 March. Since marks are often lost (see below), this may be an overestimate, but direct estimates gave approximately the same size.
Aggregation IV lasted at least 97 days. The beetles occurred on a variety of plant species, but were only occasionally seen feeding, on Tabachina longifolia. In none of the first 11 visits were any male-female pairs seen (through 23 April - each visit was during the daylight hours except on 20 March). The first pair was seen on 26 April in a group of about 600 individuals. Pairs remained rare until 16 May (four more visits), when there were more than 10 pairs in a group of 200-300 individuals, and on 21 May there were 25 pairs in a group of 85 individuals. Pairs were again relatively rare (<lo pairs among about 1,000 beetles) on 28 May. Movements of Aggregations
We were unable to understand how the beetles in aggregations (both feeding and non-feeding) coordinated their movements. Some beetles in Aggregations I and I11 walked from one aggrega- tion site to the next, but most flew. The majority of flights were <1 m. In Aggregation 111 most flights were in the direction in which the mass of beetles was moving, but this was not true in Aggrega- tion I. Both males and females in Aggregation I also initiated apparent long distance dispersal flights, flying directly upwards and away until they were lost from sight at a distance of at least 7 m. Both males and females occurred on the periphery of aggrega- tions which were on the move. A sample of the periphery of a very large (probably several thousand) feeding aggregation of M. sp. which was moving included 19 males and 29 females. A similar collection on the periphery of the non-feeding Aggregation I1 (of M. j.) yielded 13 females and 11 males.
The distances between nightly aggregation sites were 1-2 m for Aggregations 1-111. Individual beetles probably travelled much longer distances.
Behavior within a Feeding and Mating Aggregation There were small differences in the behavior of M. sp. and M. j. in Aggregation I. During nightly checks each beetle's position was classified as "central" (near or in the central mass of beetles where



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112 Psyche [VOI. 100
beetles were literally piled on each other), or "peripheral." Both male and female M. sp. were more likely to be in the central group than were individuals of M. j.: 78% of 137 male sightings and 81% of 286 female sightings of M. sp. were in the central group; corre- sponding figures for M. j. were 58% of 487 and 52% of 232 (dif- ferences between species p<.001 for both sexes; differences between sexes of the same species not significant p>.4). Resightings of marked individuals in Aggregation I suggested substantial rates of turnover in membership. For instance, 11 1 of 118 beetles (94%) had marks after the visit on the evening of 30 June, but only 51 of 90 beetles (57%) found the next night had marks. Averages of the "before and after" percentages were 88å±4 before and 57å±21 after, suggesting that about 30% of the beetles in the aggregation were new each night. Marks on caged beetles were frequently lost, however. Of 27 beetles marked with multiple dots in the afternoon, 37% had lost at least some of their marks by the evening of the next day. Thus turnover in Aggregation I was probably less than 30%. Nevertheless, substantial changes did occur. For instance at the end of the visit on the evening of 1 July, 78 of the 98 beetles present were marked; at the beginning of the visit the next night, 97 beetles (of 134) had marks. Numbers of beetles varied from night to night by up to 50%, and the relative numbers of the two species also varied, so that what was at first a nearly 50:50 mix came to be dominated by M. j. (Fig. 4). Unmarked recruits to this aggregation were more often females than males. In the period 30 June-9 July, 215 (57%) of 377 unmarked beetles found in pairs were females, while during the same period 529 (48.6%) of all sightings of marked beetles in the aggregation were females (p<.001 with Chi Squared Test). This difference may be an underestimate, since the total sightings of males probably underestimates true frequency of males because solitary individuals (some of which were not sexed for lack of marks) probably tended to be males (see below). Unless females either lost their marks much more often than males, or unmarked females failed to pair much more often than marked females, the conclusion is that females joined this aggregation at greater rates than males.




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Eberhard, Achoy, Marin & Ugalde
% solitary % M. iarnaicensis
I in pairs
OIO y. sp.
1 Days 10 15
Fig. 4. History of Aggregation I during 18 days, including numbers of beetles present each night (line), fraction of beetles in pairs (solid bars), and species com- position of the aggregation (dotted and cross-hatched bars). Pairing
Males frequently rode on females' backs both prior to and fol- lowing copulation. Riding males courted and attempted intromis- sion at irregular intervals. In the descriptions below, pairing includes all males riding on females.
Cross-specific pairs were less frequent than expected if pairing was random, even when the difference in the tendencies of the two species to be in the central area of the aggregation was taken into account. Thus of 222 sightings of paired female M. sp. in the cen- tral area on 13 nights, 32% involved a M. sp. male, while only 9% of the 105 sightings of paired M. j. females in the central portion on the same evenings involved M. sp. males (p<0.001). Corre- sponding data for the periphery were 19% of 59 sightings of paired M. sp females and 5% of 105 sightings of paired M. j. females (p=0.004).
Male M. sp in Aggregation I were more often seen unpaired than male M. j. on the same evenings (30% of 137 sightings vs. 14% of 460 sightings respectively, p<0.001), even though M. sp, females were sighted more often (291 vs 214) and the percentage



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114 Psyche [vo~. 100
of unpaired female M. sp. was slightly higher (3.4% vs. 1.9%). Male M. j. in the center were more frequently paired than those on the periphery (88% vs. 66%; p<.001). Male M. sp. showed a simi- lar, though not significant trend to pair more frequently in the ten- ter (64% vs. 51%; .2>p>.l). Percentages of paired individuals varied from night to night in the aggregation (Fig. 6). Percentages of beetles in pairs varied greatly between aggrega- tions. In the mixed Aggregation I the average was 78+10% on 12 nights, and in this aggregation most of the unpaired individuals of known sex were males (av. = 85å±16 on 11 nights with a total of 120 observations of unpaired marked individuals). Thus in Aggre- gation I nearly all female beetles were paired each night. Pairing was less frequent in some aggregations. In ten aggregations of M. sp. near Zurqui on 29 Oct. 1989 (numbers of beetledaggregation ranged from 50 to 250), five aggregations did not have a single pair, three (with 56, 75, and 100 beetles) had only 1-3 pairs, and two (with 77 and 135 beetles) had 28 and 29 pairs respectively. Substantial variation in frequency of pairing also occurred in M. j. aggregations.
Parisitism by Flies
The sarcophagid Chrysagria alticophaga Lopes and Achoy par- asitizes third instar larvae of M. j. (Lopes and Achoy 1986). In nine different collections of third instar larvae from L. octovalvis in the field, the percentage of parasitism averaged 39å±21% and undetermined numbers of flies emerged from each of three other collections of larvae from this food plant. In contrast, not a single fly emerged from more than six groups totalling >500 larvae of M. sp. collected from G. insignis.
A tachinid fly, probably Strongygaster sp., was raised from ten M. sp. collected on G. insignis near Zurqui, and (apparently the same species) from a M. j. collected near San Vito. No flies were raised from many (one hundred or more) adult M. j. collected near San Jose. A single larva emerged to pupate from each adult beetle; parasitism was fatal for the beetle.
Parasitism by Fungi
Adult M. sp. on G. insignis plants often had growths of two species of laboulbenial fungi, one on their antennae, and the other



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19931 Eberhard, Achoy, Marin & Ugalde 115 on the elytra and other body parts. Only the species apparently limited to the antenna was seen on M. j. in the field. The other species was apparently associated with more humid conditions. Individuals of M. j. kept in a moist plastic bag with infected M. sp. on a L. octovalvis plant also developed growths of this fungus. The most heavily infested individuals were M. sp. collected on G. insignis at the most humid site (near Zurqui), where beetles carry- ing >lo0 fruiting bodies were not common. The species of fungus on the antennae seemed to attack both sexes of both species of beetles with equal facility. Thus in one mixed aggregation on L. peruviana in San Pedro (collected 14 Sept. 1992), 39% of 33 M. j. and 33% of 42 M. sp. had fungal fruiting bodies on their antennae; corresponding frequencies were 33% of 43 males and 39% of 33 females.
Rates of infestation varied between sites. Thus while 93% of 29 M. sp. beetles at Zurqui had fungi on their elytra, none of 42 M. sp. near the Universidad de Costa Rica had such fungi. In a sample of 26 M. sp. from a diapausing aggregation above San Antonio de Escazu (Aggregation IV) collected at the end of the dry season (31 May 1992), 95% had fungi on their antennae, but none had fungi on the rest of their bodies.
Presumably the fungi caused little damage to the beetles (Bal- azuc 1988), though occasionally fruiting bodies occurred on the ventral surfaces of tarsomeres, and must have caused some diffi- culty in maintaining footholds.
The two species of this study (as well as an additional Macro- haltica species from Colombia - Eberhard unpub.) are unusual in forming aggregations, sometimes quite tightly grouped, of up to several thousand individuals. Altica adults occasionally occur in small groups (e.g. Phillips 1977a found A. lythri in the spring in groups of 6-12 and occasionally up to 40 beetles, and groups of A. oleracea were smaller; Baker et al. 1972 mention a "tendency to aggregate" in Haltica carduorum). The function or functions of the aggregations are not clear. Phillips (1977a) and Baker et al. (1972) proposed that they serve to bring males and females together. The slightly larger numbers of males in most aggregations of M. j. and M. sp., and the apparently greater turnover of females than males



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1 16 Psyche [VOI. 100
in Aggregation I are in accord with this idea. Some aggregations, however, had little or no mating activity, and females had undevel- oped ovaries, so this cannot be the only function. Another possible function could be to overwhelm the defensive responses of food plants by attacking en mass. This explanation cannot easily account for the non-feeding aggregations found far from food plants. A further possibility is that the metallic colors of these bee- tles are aposematic, and that aggregations make this signal more obvious. These possible functions are not mutually exclusive. Data on beetles marked with paint or with fungal growth permit glimpses of their movement patterns. At least some aggregations (Aggregation I) showed substantial rates of turnover in member- ship. Some beetles which had left this aggregation subsequently returned, raising the possibility that individuals may circulate between different aggregations. The general failure of M. sp. with heavy loads of fungi (typical of beetles near Zurqui) to appear at other sites (the farthest sighting was near San Isidro de Heredia, approximately 4 km away) suggests that longer distance move- ments may be rare (at least in this species, and of those individuals (older?) with large accumulations of fungi). Some of the differences between the behavior of M. sp. and M. j. adults within a feeding aggregation may be related to differences between food plant species. Unmixed aggregations of M. sp. on the very large G. insignis leaves (Fig. 2) usually take many days (prob- ably on the order of a week) to move on to another leaf. On the other hand, aggregations of M. j. on Ludwigia spp. can completely destroy small plants in a day or less, and are thus more often obliged to move on. The greater tendency of M. j. in a mixed aggregation to move away from the center may be related to this difference.
Some non-feeding aggregations, in which females had only weakly developed ovaries and the beetles were not soft and recently emerged, suggest that both species may undergo reproduc- tive diapause, as occurs in some temperate zone chrysomelids (e.g. Waloff and Richards 1958). Most of the food plants (except T. longifolia and G. insignis) are somewhat seasonal, with reduced growth and population sizes during the dry season in most sites. Perhaps poor feeding soon after emergence above ground, which we have shown to inhibit ovary development in females and sexual



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Eberhard, Achoy, Marin & Ugalde
behavior in males, causes beetles to enter reproductive diapause. Such feeding regimes probably occur in nature when adults emerge at sites where aggregations of adults and larvae have destroyed the food plants. Diapause is probably facultative. We found groups of mature larvae feeding on L. octovalvis plants late in the dry season (29 April 1992), and aggregations of M. sp. occur on G. insignis year round.
It is clear that even for M. sp., the plant G. insignis is relatively "difficult." Larvae raised in captivity took 1.6 times longer to mature, and at maturity weighed on average only 71% as much as larvae of the same species raised on L. octovalvis. Females of M. sp. laid on average 4.8 times more eggs when fed L. octovalvis than when fed G. insignis. Possible compensating advantages of G. insignis are that it is relatively non-seasonal, and grows in cooler climates (i.e. it could have served as a refuge during glaciations). Although M. j. and M. sp. are interfertile, producing hybrids which are also fertile (R. Achoy, unpub.), and although cross-spe- cific male-female pairs are common in nature, there are several reasons to believe that the two forms represent distinct species: male genitalia differ in form (Eberhard and Achoy in prep.); an elytral carina is present in females of M. sp. but is less pronounced in those of M. j. (W. Eberhard unpub.); abilities to develop on dif- ferent species of food plant are different (this study); male-female pairs tend to be conspecific in mixed aggregations (this study); clustering behavior within an aggregation differs (this study); male copulation behavior differs (Eberhard and Kariko in prep.); and offspring of females which have mated with both types of males tend to be fathered by the conspecific male (Eberhard and Ugalde in prep.). The beetles' preference for highly disturbed habitats makes it impossible to determine whether or not these species evolved in isolation and have only recently come into contact due to the extensive human modification of their habitats. The ranges of two interspecifically fertile species of Macro- haltica beetles overlap in central Costa Rica. Some species of food plant were used by both species, others by only one. The two species differed in their abilities to develop on different food plants. Adults of both beetle species tended to occur in large



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118 Psyche [vo~. 100
aggregations. Feeding and mating were common in some aggrega- tions, while in others beetles were in apparent reproductive dia- pause. Beetles in mixed aggregations tended to pair with conspecifics, but many cross-specific pairs also occurred. Although aggregations moved slowly from one host plant to another, mem- bership within at least some aggregations showed substantial turnover. Other aspects of the beetles' natural history, including oviposition behavior, defensive behavior, development and behav- ior of immatures, dipterous parasites, and fungal infections of adults are also described.
We thank David Furth, J. Santisteban, S. L. Shute, and Richard White for beetle identifications and other helpful information, Peter Dobbler for help with the fungi, Mahmut Sosa for observa- tions of lizards, Rafael Lucas Rodriguez for specimens, and Jorge Gomez Laurito and Peter Raven for plant identifications. Fernando Cortkz granted permission to study beetles in Parque Nacional Braulio Carrillo. JU was supported by an Exxon Fellowship from the Smithsonian Tropical Research Institute. The Vicerrectoria de Investigacih of the Universidad de Costa Rica and STRI also pro- vided financial support.
BAKER, C. R. B., BLACKMAN, R. L., AND CLARIDGE, M. F. 1972. Studies on Haltica carduorum Guerin (Coleoptera, Chrysomelidae), an alien beetle released in Britain as a contribution to the biological con- trol of creeping thistle, Cirsium arvense (L.) Scop. J. Appl. Ecol. 9: 8 19-830.
BALAZUC, J.
1988. Laboulbeniales (Ascomycetes) parasitic on Chrysomelidae, p. 389-398 in P. Jolivet, E. Petitpierre and T. H. Hsiao (eds.) Biology of Chrysomelidae. Kluwer Academic Publ.
BALSBAUGH, E. U. AND HAYS, K. L.
1972. The leaf beetles of Alabama (Coleoptera: Chrysomelidae). Bull. Agric. Expt. Sta. Auburn Univ. 441: 1-223.
BARSTOW, D. A. AND GITTINS, A. R.
1973. Descriptions of the life stage of Altica bimarginata Say (Coleoptera: Chrysomelidae). J. Kans. Ent. Soc. 46: 500-5 10. FERNANDEZ, D.
1984. Estudio anatomic0 y morfol6gico de Gunnera insignis (Oerst.) A. DC. Rev. Biol. Trop. 32: 197-202.




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19931 Eberhard, Achoy, Marin & Ugalde 119 JOLIVET, P.
1988. Food habits and food selection of Chrysomelidae. Bionomic and evolu- tionary perspectives. p. 1-24 in P. Jolivet, E. Petitpierre and T. H. Hsaio (eds.) Biology of Chrysomelidae. Kluwer Academic Publ. KING, A. AND SAUNDERS. J.
1984. Las plagas invertebradas de cultivos anuales alimenticios en America Central. Overseas Dev. Administ. London 1-1 82. LESAGE, L.
1990. Description of a new Canadian species of Altica feeding on birch (Coleoptera: Chrysomelidae, Alticinae). Can. Ent. 122: 1229-1 234. LOPES, H. DE S., AND ACHOY, R. M.
1986. On Chrysagria (Diptera, Sarcophagidae) with descriptions of two new species, one of them living on the larvae of Altica sp. (Coleoptera, Chrysomelidae). Rev. Brasil. Biol. 46: 273-276. PHILLIPS, W. M.
1977a. Observations on the biology and ecology of the chrysomelid genus Haltica Geoff. in Britain. Ecol. Entom. 2: 205-216. 1977b.Some aspects of the host plant relations of the chrysomelid genus Haltica with special reference to Haltica lythri. Ent. exp. appl. 21: 261-274.
1978. Sensilla types from the ovipositor of the flea beetle Altica lythri (Coleoptera: Chrysomelidae). Ent. exp. appl. 24: 399-400. 1979. A contribution to the study of species relations within the chrysomelid genus Altica Muller in Britain. Zool. J. Linn. Soc. 66: 289-308. SCHERER, G.
1969. Die Alticinae des Indischen Subkontinentes. Pac. Ins. Monogr. 22: 1-251.
WALOFF, N. AND RICHARDS, 0. W.
1958. The biology of the chrysomelid beetle, Phytodecta olivacea (Forster) (Coleoptera: Chrysomelidae). Trans. Roy. Ent. Soc. Lond. 110: 99-1 16. WOODS, W. C.
1917. The biology of the alder flea-beetle. Maine Agric. Expt. Sta. 265: 249-284.
1918. The biology of Maine species of Altica. Maine Agric. Expt. Sta. 273: 149-204.




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Volume 100 table of contents